Michael Anderson | University of Cambridge (original) (raw)

Papers by Michael Anderson

Research paper thumbnail of Successfully controlling intrusive memories is harder when control must be sustained

After unpleasant events, people often experience intrusive memories that undermine their peace of... more After unpleasant events, people often experience intrusive memories that undermine their peace of mind. In response, they often suppress these unwanted memories from awareness. Such efforts may fail, however, when inhibitory control demands are high due to the need to sustain control, or when fatigue compromises inhibitory capacity. Here we examined how sustained inhibitory demand affected intrusive memories in the Think/No-Think paradigm. To isolate intrusions, participants reported, trial-by-trial, whether their preceding attempt to suppress retrieval had triggered retrieval of the memory they intended to suppress. Such counter-intentional retrievals provide a laboratory model of the sort of involuntary retrieval that may underlie intrusive memories. Using this method, we found that longer duration trials increased the probability of an intrusion. Moreover, on later No-Think trials, control over intrusions suddenly declined, with longer trial durations triggering more relapses of items that had been previously been purged. Thus, the challenges of controlling retrieval appear to cause a decline in control over time, due to a change in state, such as fatigue. These findings raise the possibility that characteristics often true of people with psychiatric disorders – such as compromised sleep, and increased demand on control – may contribute to difficulties in suppressing intrusive memories.

Research paper thumbnail of The origins of repetitive thought in rumination: Separating cognitive style from deficits in inhibitory control over memory

Journal of Behavior Therapy and Experimental Psychiatry, 2015

Background and objectives: Rumination is a major contributor to the maintenance of affective diso... more Background and objectives: Rumination is a major contributor to the maintenance of affective disorders and has been linked to memory control deficits. However, ruminators often report intentionally engaging in repetitive thought due to its perceived benefits. Deliberate re-processing may lead to the appearance of a memory control deficit that is better explained as a difference in cognitive style. Methods: Ninety-six undergraduate students volunteered to take part in a direct-suppression variant of the Think/No-Think paradigm after which they completed self-report measures of rumination and the degree to which they deliberately re-processed the to-be-suppressed items. Results: We demonstrate a relation between rumination and impaired suppression-induced forgetting. This relation is robust even when controlling for deliberate re-processing of the to-be-suppressed items, a behavior itself related to both rumination and suppression. Therefore, whereas conscious fixation on to-be-suppressed items reduced memory suppression, it did not fully account for the relation between rumination and memory suppression. Limitations: The current experiment employed a retrospective measure of deliberate re-processing in the context of an unscreened university sample; future research might therefore generalize our findings using an online measure of deliberate re-processing or within a clinical population. Conclusions: We provide evidence that deliberate re-processing accounts for some e but not all e of the relation between rumination and suppression-induced forgetting. The present findings, observed in a paradigm known to engage top-down inhibitory modulation of mnemonic processing, provide the most theoretically focused evidence to date for the existence of a memory control deficit in rumination.

Research paper thumbnail of Failing to Forget: Inhibitory-Control Deficits Compromise Memory Suppression in Posttraumatic Stress Disorder

Psychological science, Jan 6, 2015

Most people have experienced distressing events that they would rather forget. Although memories ... more Most people have experienced distressing events that they would rather forget. Although memories of such events become less intrusive with time for the majority of people, those with posttraumatic stress disorder (PTSD) are afflicted by vivid, recurrent memories of their trauma. Often triggered by reminders in the daily environment, these memories can cause severe distress and impairment. We propose that difficulties with intrusive memories in PTSD arise in part from a deficit in engaging inhibitory control to suppress episodic retrieval. We tested this hypothesis by adapting the think/no-think paradigm to investigate voluntary memory suppression of aversive scenes cued by naturalistic reminders. Retrieval suppression was compromised significantly in PTSD patients, compared with trauma-exposed control participants. Furthermore, patients with the largest deficits in suppression-induced forgetting were also those with the most severe PTSD symptoms. These results raise the possibility ...

Research paper thumbnail of Inducing amnesia through systemic suppression

Hippocampal damage profoundly disrupts the ability to store new memories of life events. Amnesic ... more Hippocampal damage profoundly disrupts the ability to store new memories of life events. Amnesic windows might also occur in healthy people due to disturbed hippocampal function arising during mental processes that systemically reduce hippocampal activity. Intentionally suppressing memory retrieval (retrieval stopping) reduces hippocampal activity via control mechanisms mediated by the lateral prefrontal cortex. Here we show that when people suppress retrieval given a reminder of an unwanted memory, they are considerably more likely to forget unrelated experiences from periods surrounding suppression. This amnesic shadow follows a dose-response function, becomes more pronounced after practice suppressing retrieval, exhibits characteristics indicating disturbed hippocampal function, and is predicted by reduced hippocampal activity. These findings indicate that stopping retrieval engages a suppression mechanism that broadly compromises hippocampal processes and that hippocampal stabilization processes can be interrupted strategically. Cognitively triggered amnesia constitutes an unrecognized forgetting process that may account for otherwise unexplained memory lapses following trauma.

Research paper thumbnail of Remembering can cause forgetting: Retrieval dynamics in long-term memory

Journal of Experimental Psychology: Learning, Memory, and Cognition, 1994

Three studies show that the retrieval process itself causes long-lasting forgetting. Ss studied 8... more Three studies show that the retrieval process itself causes long-lasting forgetting. Ss studied 8 categories (e.g., Fruit). Half the members of half the categories were then repeatedly practiced through retrieval tests (e.g., Fruit Or_____). Category-cued recall of unpracticed members of practiced categories was impaired on a delayed test. Experiments 2 and 3 identified 2 significant features of this retrieval-induced forgetting: The impairment remains when output interference is controlled, suggesting a retrieval-based suppression that endures for 20 min or more, and the impairment appears restricted to high-frequency members. Low-frequency members show little impairment, even in the presence of strong, practiced competitors that might be expected to block access to those items. These findings suggest a critical role for suppression in models of retrieval inhibition and implicate the retrieval process itself in everyday forgetting.

Research paper thumbnail of Selection and stopping in voluntary action: A meta-analysis and combined fMRI study

NeuroImage, 2014

Voluntary action control requires selection of appropriate responses and stopping of inappropriat... more Voluntary action control requires selection of appropriate responses and stopping of inappropriate responses. Selection and stopping are often investigated separately, but they appear to recruit similar brain regions, including the pre-supplementary motor area (preSMA) and inferior frontal gyrus. We therefore examined the evidence for overlap of selection and stopping using two approaches: a meta-analysis of existing studies of selection and stopping, and a novel within-subject fMRI study in which action selection and a stop signal task were combined factorially. The novel fMRI study also permitted us to investigate hypotheses regarding a common mechanism for selection and stopping. The preSMA was identified by both methods as common to selection and stopping. However, stopping a selected action did not recruit preSMA more than stopping a specified action, nor did stop signal reaction times differ significantly across the two conditions. These findings suggest that the preSMA supports both action selection and stopping, but the two processes may not require access to a common inhibition mechanism. Instead, the preSMA might represent information about potential actions that is used in both action selection and stopping in order to resolve conflict between competing available responses.

Research paper thumbnail of The prefrontal cortex achieves inhibitory control by facilitating subcortical motor pathway connectivity

The Journal of neuroscience : the official journal of the Society for Neuroscience, Jan 14, 2015

Communication between the prefrontal cortex and subcortical nuclei underpins the control and inhi... more Communication between the prefrontal cortex and subcortical nuclei underpins the control and inhibition of behavior. However, the interactions in such pathways remain controversial. Using a stop-signal response inhibition task and functional imaging with analysis of effective connectivity, we show that the lateral prefrontal cortex influences the strength of communication between regions in the frontostriatal motor system. We compared 20 generative models that represented alternative interactions between the inferior frontal gyrus, presupplementary motor area (preSMA), subthalamic nucleus (STN), and primary motor cortex during response inhibition. Bayesian model selection revealed that during successful response inhibition, the inferior frontal gyrus modulates an excitatory influence of the preSMA on the STN, thereby amplifying the downstream polysynaptic inhibition from the STN to the motor cortex. Critically, the strength of the interaction between preSMA and STN, and the degree o...

Research paper thumbnail of Failing to Forget: Inhibitory-Control Deficits Compromise Memory Suppression in Posttraumatic Stress Disorder.

Most people have experienced distressing events that they would rather forget. Although memories ... more Most people have experienced distressing events that they would rather forget. Although memories of such events
become less intrusive with time for the majority of people, those with posttraumatic stress disorder (PTSD) are afflicted
by vivid, recurrent memories of their trauma. Often triggered by reminders in the daily environment, these memories
can cause severe distress and impairment. We propose that difficulties with intrusive memories in PTSD arise in part
from a deficit in engaging inhibitory control to suppress episodic retrieval. We tested this hypothesis by adapting
the think/no-think paradigm to investigate voluntary memory suppression of aversive scenes cued by naturalistic
reminders. Retrieval suppression was compromised significantly in PTSD patients, compared with trauma-exposed
control participants. Furthermore, patients with the largest deficits in suppression-induced forgetting were also those
with the most severe PTSD symptoms. These results raise the possibility that prefrontal mechanisms supporting
inhibitory control over memory are impaired in PTSD.

Research paper thumbnail of Retrieval induces adaptive forgetting of competing memories via cortical pattern suppression

Remembering a past experience can, surprisingly, cause forgetting. Forgetting arises when other c... more Remembering a past experience can, surprisingly, cause forgetting. Forgetting arises when other competing traces interfere with retrieval and inhibitory control mechanisms are engaged to suppress the distraction they cause. This form of forgetting is considered to be adaptive because it reduces future interference. The effect of this proposed inhibition process on competing memories has, however, never been observed, as behavioral methods are ‘blind’ to retrieval dynamics and neuroimaging methods have not isolated retrieval of individual memories. We developed a canonical template tracking method to quantify the activation state of individual target memories and competitors during retrieval. This method revealed that repeatedly retrieving target memories suppressed cortical patterns unique to competitors. Pattern suppression was related to engagement of prefrontal regions that have been implicated in resolving retrieval competition and, critically, predicted later forgetting. Thus, our findings demonstrate a cortical pattern suppression mechanism through which remembering adaptively shapes which aspects of our past remain accessible.

Research paper thumbnail of Older Adults Can Suppress Unwanted Memories When Given an Appropriate Strategy

Memory suppression refers to the ability to exclude distracting memories from conscious awareness... more Memory suppression refers to the ability to exclude distracting memories from conscious awareness, and this ability can be assessed with the think/no-think paradigm. Recent research with older adults has provided evidence suggesting both intact and deficient memory suppression. The present studies seek to understand the conditions contributing to older adults’ ability to suppress memories voluntarily. We report 2 experiments
indicating that the specificity of the think/no-think task instructions contributes to older adults’ suppression
success: When older adults receive open-ended instructions that require them to develop a retrieval suppression
strategy on their own, they show diminished memory suppression compared with younger adults. Conversely, when older adults receive focused instructions directing them to a strategy thought to better isolate inhibitory control, they show suppression-induced forgetting similar to that exhibited by younger adults. Younger adults demonstrate memory suppression regardless of the specificity of the instructions given, suggesting that the ability to select a successful suppression strategy spontaneously may be compromised in
older adults. If so, this deficit may be associated with diminished control over unwanted memories in naturalistic settings if impeded strategy development reduces the successful deployment of inhibitory control.

Research paper thumbnail of The Prefrontal Cortex Achieves Inhibitory Control by Facilitating Subcortical Motor Pathway Connectivity

Communication between the prefrontal cortex and subcortical nuclei underpins the control and inhi... more Communication between the prefrontal cortex and subcortical nuclei underpins the control and inhibition of behavior. However, the interactions in such pathways remain controversial. Using a stop-signal response inhibition task and functional imaging with analysis of effective connectivity, we show that the lateral prefrontal cortex influences the strength of communication between regions in the frontostriatal motor system. We compared 20 generative models that represented alternative interactions between the inferior frontal gyrus, presupplementary motor area (preSMA), subthalamic nucleus (STN), and primary motor cortex during response inhibition.
Bayesian model selection revealed that during successful response inhibition, the inferior frontal gyrus modulates an excitatory influence of the preSMA on the STN, thereby amplifying the downstream polysynaptic inhibition from the STN to the motor cortex. Critically, the strength of the interaction between preSMA and STN, and the degree of modulation by the inferior frontal gyrus, predicted individual
differences in participants’ stopping performance (stop-signal reaction time). We then used diffusion-weighted imaging with tractography to assess white matter structure in the pathways connecting these three regions. The mean diffusivity in tracts between preSMA and the STN, and between the inferior frontal gyrus and STN, also predicted individual differences in stopping efficiency. Finally, we found that white matter structure in the tract between preSMA and STN correlated with effective connectivity of the same pathway, providing important cross-modal validation of the effective connectivity measures. Together, the results demonstrate the network dynamics and
modulatory role of the prefrontal cortex that underpin individual differences in inhibitory control.

Research paper thumbnail of Adaptive Top–Down Suppression of Hippocampal Activity and the Purging of Intrusive Memories from Consciousness

When reminded of unwanted memories, people often attempt to suppress these experiences from aware... more When reminded of unwanted memories, people often
attempt to suppress these experiences from awareness. Prior
work indicates that control processes mediated by the dorsolateral prefrontal cortex (DLPFC) modulate hippocampal activity during such retrieval suppression. It remains unknown whether this modulation plays a role in purging an intrusive memory from consciousness. Here, we combined fMRI and effective connectivity analyses with phenomenological reports to scrutinize a role for adaptive top–down suppression of hippocampal retrieval processes in terminating mnemonic awareness of intrusive memories. Participants either suppressed or recalled memories of pictures depicting faces or places. After each trial, they reported their success at regulating awareness of the memory. DLPFC activation was greatest when unwanted memories intruded into consciousness and needed to be purged, and this increased engagement predicted superior control of intrusive memories over time. However, hippocampal activity was decreased during the suppression
of place memories only. Importantly, the inhibitory
influence of the DLPFC on the hippocampus was linked to the
ensuing reduction in intrusions of the suppressed memories.
Individuals who exhibited negative top–down coupling during
early suppression attempts experienced fewer involuntary memory intrusions later on. Over repeated suppressions, the DLPFC–hippocampus connectivity grew less negative with the degree that they no longer had to purge unwanted memories from awareness. These findings support a role of DLPFC in countermanding the unfolding recollection of an unwanted memory
via the suppression of hippocampal processing, a mechanism
that may contribute to adaptation in the aftermath of traumatic
experiences.

Research paper thumbnail of The origins of repetitive thought in rumination: Separating cognitive style from deficits in inhibitory control over memory

Background and objectives: Rumination is a major contributor to the maintenance of affective diso... more Background and objectives: Rumination is a major contributor to the maintenance of affective disorders
and has been linked to memory control deficits. However, ruminators often report intentionally engaging
in repetitive thought due to its perceived benefits. Deliberate re-processing may lead to the appearance
of a memory control deficit that is better explained as a difference in cognitive style.
Methods: Ninety-six undergraduate students volunteered to take part in a direct-suppression variant of
the Think/No-Think paradigm after which they completed self-report measures of rumination and the
degree to which they deliberately re-processed the to-be-suppressed items.
Results: We demonstrate a relation between rumination and impaired suppression-induced forgetting.
This relation is robust even when controlling for deliberate re-processing of the to-be-suppressed items,
a behavior itself related to both rumination and suppression. Therefore, whereas conscious fixation on
to-be-suppressed items reduced memory suppression, it did not fully account for the relation between
rumination and memory suppression.
Limitations: The current experiment employed a retrospective measure of deliberate re-processing in the
context of an unscreened university sample; future research might therefore generalize our findings
using an online measure of deliberate re-processing or within a clinical population.
Conclusions: We provide evidence that deliberate re-processing accounts for some e but not all e of the
relation between rumination and suppression-induced forgetting. The present findings, observed in a
paradigm known to engage top-down inhibitory modulation of mnemonic processing, provide the most
theoretically focused evidence to date for the existence of a memory control deficit in rumination.

Research paper thumbnail of Examining the costs and benefits of inhibition in memory retrieval

Inhibitory control is thought to serve an adaptive function in controlling behavior, with individ... more Inhibitory control is thought to serve an adaptive function in controlling behavior, with individual differences predicting variation in numerous cognitive functions. However, inhibition is more properly construed as inducing both benefits and costs to performance. Benefits arise at the point when inhibition prevents expression of an unwanted or contextually inappropriate response; costs arise later, when access to the inhibited representation is
required by other processes. Here we illustrate how failure to consider both the costs and benefits of inhibition has generated confusion in the literature on individual differences
in cognitive control. Using retrieval-induced forgetting as a model case, we illustrate this by showing that changing the way that retrieval-induced forgetting is measured to allow greater expression of the benefits of inhibition together with the costs can reduce and even reverse the theoretically predicted correlation between motor and memory inhibition. Specifically, we show that when the final test in a retrieval-induced forgetting procedure employs item-specific cues (i.e., category-plus-stem cued recall and item-recognition) that better isolate the lingering costs of inhibition, better motor response inhibition (faster stop-signal reaction times) predicts greater retrieval-induced forgetting. In striking contrast, when the final test is less well controlled, allowing both the costs and benefits of inhibition to contribute, motor response inhibition has the opposite relationship with retrieval-induced forgetting. These findings underscore the importance of considering the correlated costs and benefits problem when studying individual differences in inhibitory control. More generally, they suggest that a shared inhibition mechanism may underlie
people’s ability to control memories and actions.

Research paper thumbnail of Direct suppression as a mechanism for controlling unpleasant memories in daily life

Suppressing unwanted memories can impair their later recall. Recent work shows that this forgetti... more Suppressing unwanted memories can impair their later recall. Recent work shows that this forgetting is achieved by at least two mechanisms supported by distinct neural systems: thought substitution and direct suppression (Benoit & Anderson, 2012). Here, we examined whether direct suppression, thought to be
achieved by down-regulation of hippocampal activity, can disrupt memory of aversive scenes, and, if so,whether this disruption is linked to people’s perception of their ability to control intrusive thoughts. We presented participants with strong naturalistic reminders to aversive scenes and asked them to either
covertly retrieve or directly suppress the associated scenes. Later, participants were cued with the reminders and asked to recall the scenes in detail. Direct suppression reduced recall probability of the
scenes and also reduced the number of details recalled, even when scenes were remembered. Deficits in recall arose for minor details but also for details central to each scene’s gist. Participants with higher self-perceived control abilities over intrusive thoughts showed greater forgetting than did those reporting lower levels of control. These findings suggest that inhibitory processes underlying direct suppression can disrupt retention of aversive visual memories and link those processes to individual differences in
control over intrusive thoughts in everyday life. These findings reinforce the possibility that inhibition may be less efficient in people likely to acquire posttraumatic stress disorder in the wake of a traumatic experience.

Research paper thumbnail of Neural mechanisms of Motivated Forgetting

Not all memories are equally welcome in awareness. People limit the time they spend thinking abo... more Not all memories are equally welcome in awareness.
People limit the time they spend thinking about unpleasant
experiences, a process that begins during encoding,
but that continues when cues later remind someone of
the memory. Here, we review the emerging behavioural
and neuroimaging evidence that suppressing awareness
of an unwelcome memory, at encoding or retrieval, is
achieved by inhibitory control processes mediated by
the lateral prefrontal cortex. These mechanisms interact
with neural structures that represent experiences in
memory, disrupting traces that support retention. Thus,
mechanisms engaged to regulate momentary awareness
introduce lasting biases in which experiences remain
accessible. We argue that theories of forgetting
that neglect the motivated control of awareness omit a
powerful force shaping the retention of our past.

Research paper thumbnail of Suppressing unwanted memories reduces their unconscious influence via targeted cortical inhibition

Suppressing retrieval of unwanted memories reduces their later conscious recall. It is widely be... more Suppressing retrieval of unwanted memories reduces their later
conscious recall. It is widely believed, however, that suppressed
memories can continue to exert strong unconscious effects that
may compromise mental health. Here we show that excluding
memories from awareness not only modulates medial temporal
lobe regions involved in explicit retention, but also neocortical
areas underlying unconscious expressions of memory. Using
repetition priming in visual perception as a model task, we found
that excluding memories of visual objects from consciousness
reduced their later indirect influence on perception, literally making
the content of suppressed memories harder for participants to
see. Critically, effective connectivity and pattern similarity analysis
revealed that suppression mechanisms mediated by the right
middle frontal gyrus reduced activity in neocortical areas involved
in perceiving objects and targeted the neural populations most
activated by reminders. The degree of inhibitory modulation of
the visual cortex while people were suppressing visual memories
predicted, in a later perception test, the disruption in the neural
markers of sensory memory. These findings suggest a neurobiological model of how motivated forgetting affects the unconscious expression of memory that may be generalized to other types of memory content. More generally, they suggest that the century old assumption that suppression leaves unconscious memories intact should be reconsidered.

Research paper thumbnail of Suppressing unwanted memories by executive control

Freud proposed that unwanted memories can be forgotten by pushing them into the unconscious, a pr... more Freud proposed that unwanted memories can be forgotten by pushing them into the unconscious, a process called repression1. The existence of repression has remained controversial for more than a century, in part because of its strong coupling with trauma, and the ethical and practical difficulties of studying such processes in controlled experiments. However, behavioural and neurobiological research on memory and attention shows that people have executive control processes directed at minimizing perceptual distraction2, 3, overcoming interference during short and long-term memory tasks3, 4, 5, 6, 7 and stopping strong habitual responses to stimuli8, 9, 10, 11, 12, 13. Here we show that these mechanisms can be recruited to prevent unwanted declarative memories from entering awareness, and that this cognitive act has enduring consequences for the rejected memories. When people encounter cues that remind them of an unwanted memory and they consistently try to prevent awareness of it, the later recall of the rejected memory becomes more difficult. The forgetting increases with the number of times the memory is avoided, resists incentives for accurate recall and is caused by processes that suppress the memory itself. These results show that executive control processes not uniquely tied to trauma may provide a viable model for repression.

Research paper thumbnail of Neural systems underlying the suppression of unwanted memories

Over a century ago, Freud proposed that unwanted memories can be excluded from awareness, a proc... more Over a century ago, Freud proposed that unwanted memories can be excluded
from awareness, a process called repression. It is unknown, however, how
repression occurs in the brain. We used functional magnetic resonance imaging
to identify the neural systems involved in keeping unwanted memories out of
awareness. Controlling unwanted memories was associated with increased
dorsolateral prefrontal activation, reduced hippocampal activation, and impaired
retention of those memories. Both prefrontal cortical and right hippocampal
activations predicted the magnitude of forgetting. These results
confirm the existence of an active forgetting process and establish a neurobiological
model for guiding inquiry into motivated forgetting.

Research paper thumbnail of Opposing mechanisms support the voluntary forgetting of unwanted memories

Reminders of the past can trigger the recollection of events that one would rather forget. Here,... more Reminders of the past can trigger the recollection of
events that one would rather forget. Here, using
fMRI, we demonstrate two distinct neural mechanisms
that foster the intentional forgetting of such
unwanted memories. Both mechanisms impair
long-term retention by limiting momentary awareness
of the memories, yet they operate in opposite
ways. One mechanism, direct suppression, disengages
episodic retrieval through the systemic inhibition
of hippocampal processing that originates
from right dorsolateral prefrontal cortex (PFC). The
opposite mechanism, thought substitution, instead
engages retrieval processes to occupy the limited
focus of awareness with a substitute memory. It is
mediated by interactions between left caudal and
midventrolateral PFC that support the selective
retrieval of substitutes in the context of prepotent,
unwanted memories. These findings suggest that
we are not at the mercy of passive forgetting; rather,
our memories can be shaped by two opposite mechanisms
of mnemonic control.

Research paper thumbnail of Successfully controlling intrusive memories is harder when control must be sustained

After unpleasant events, people often experience intrusive memories that undermine their peace of... more After unpleasant events, people often experience intrusive memories that undermine their peace of mind. In response, they often suppress these unwanted memories from awareness. Such efforts may fail, however, when inhibitory control demands are high due to the need to sustain control, or when fatigue compromises inhibitory capacity. Here we examined how sustained inhibitory demand affected intrusive memories in the Think/No-Think paradigm. To isolate intrusions, participants reported, trial-by-trial, whether their preceding attempt to suppress retrieval had triggered retrieval of the memory they intended to suppress. Such counter-intentional retrievals provide a laboratory model of the sort of involuntary retrieval that may underlie intrusive memories. Using this method, we found that longer duration trials increased the probability of an intrusion. Moreover, on later No-Think trials, control over intrusions suddenly declined, with longer trial durations triggering more relapses of items that had been previously been purged. Thus, the challenges of controlling retrieval appear to cause a decline in control over time, due to a change in state, such as fatigue. These findings raise the possibility that characteristics often true of people with psychiatric disorders – such as compromised sleep, and increased demand on control – may contribute to difficulties in suppressing intrusive memories.

Research paper thumbnail of The origins of repetitive thought in rumination: Separating cognitive style from deficits in inhibitory control over memory

Journal of Behavior Therapy and Experimental Psychiatry, 2015

Background and objectives: Rumination is a major contributor to the maintenance of affective diso... more Background and objectives: Rumination is a major contributor to the maintenance of affective disorders and has been linked to memory control deficits. However, ruminators often report intentionally engaging in repetitive thought due to its perceived benefits. Deliberate re-processing may lead to the appearance of a memory control deficit that is better explained as a difference in cognitive style. Methods: Ninety-six undergraduate students volunteered to take part in a direct-suppression variant of the Think/No-Think paradigm after which they completed self-report measures of rumination and the degree to which they deliberately re-processed the to-be-suppressed items. Results: We demonstrate a relation between rumination and impaired suppression-induced forgetting. This relation is robust even when controlling for deliberate re-processing of the to-be-suppressed items, a behavior itself related to both rumination and suppression. Therefore, whereas conscious fixation on to-be-suppressed items reduced memory suppression, it did not fully account for the relation between rumination and memory suppression. Limitations: The current experiment employed a retrospective measure of deliberate re-processing in the context of an unscreened university sample; future research might therefore generalize our findings using an online measure of deliberate re-processing or within a clinical population. Conclusions: We provide evidence that deliberate re-processing accounts for some e but not all e of the relation between rumination and suppression-induced forgetting. The present findings, observed in a paradigm known to engage top-down inhibitory modulation of mnemonic processing, provide the most theoretically focused evidence to date for the existence of a memory control deficit in rumination.

Research paper thumbnail of Failing to Forget: Inhibitory-Control Deficits Compromise Memory Suppression in Posttraumatic Stress Disorder

Psychological science, Jan 6, 2015

Most people have experienced distressing events that they would rather forget. Although memories ... more Most people have experienced distressing events that they would rather forget. Although memories of such events become less intrusive with time for the majority of people, those with posttraumatic stress disorder (PTSD) are afflicted by vivid, recurrent memories of their trauma. Often triggered by reminders in the daily environment, these memories can cause severe distress and impairment. We propose that difficulties with intrusive memories in PTSD arise in part from a deficit in engaging inhibitory control to suppress episodic retrieval. We tested this hypothesis by adapting the think/no-think paradigm to investigate voluntary memory suppression of aversive scenes cued by naturalistic reminders. Retrieval suppression was compromised significantly in PTSD patients, compared with trauma-exposed control participants. Furthermore, patients with the largest deficits in suppression-induced forgetting were also those with the most severe PTSD symptoms. These results raise the possibility ...

Research paper thumbnail of Inducing amnesia through systemic suppression

Hippocampal damage profoundly disrupts the ability to store new memories of life events. Amnesic ... more Hippocampal damage profoundly disrupts the ability to store new memories of life events. Amnesic windows might also occur in healthy people due to disturbed hippocampal function arising during mental processes that systemically reduce hippocampal activity. Intentionally suppressing memory retrieval (retrieval stopping) reduces hippocampal activity via control mechanisms mediated by the lateral prefrontal cortex. Here we show that when people suppress retrieval given a reminder of an unwanted memory, they are considerably more likely to forget unrelated experiences from periods surrounding suppression. This amnesic shadow follows a dose-response function, becomes more pronounced after practice suppressing retrieval, exhibits characteristics indicating disturbed hippocampal function, and is predicted by reduced hippocampal activity. These findings indicate that stopping retrieval engages a suppression mechanism that broadly compromises hippocampal processes and that hippocampal stabilization processes can be interrupted strategically. Cognitively triggered amnesia constitutes an unrecognized forgetting process that may account for otherwise unexplained memory lapses following trauma.

Research paper thumbnail of Remembering can cause forgetting: Retrieval dynamics in long-term memory

Journal of Experimental Psychology: Learning, Memory, and Cognition, 1994

Three studies show that the retrieval process itself causes long-lasting forgetting. Ss studied 8... more Three studies show that the retrieval process itself causes long-lasting forgetting. Ss studied 8 categories (e.g., Fruit). Half the members of half the categories were then repeatedly practiced through retrieval tests (e.g., Fruit Or_____). Category-cued recall of unpracticed members of practiced categories was impaired on a delayed test. Experiments 2 and 3 identified 2 significant features of this retrieval-induced forgetting: The impairment remains when output interference is controlled, suggesting a retrieval-based suppression that endures for 20 min or more, and the impairment appears restricted to high-frequency members. Low-frequency members show little impairment, even in the presence of strong, practiced competitors that might be expected to block access to those items. These findings suggest a critical role for suppression in models of retrieval inhibition and implicate the retrieval process itself in everyday forgetting.

Research paper thumbnail of Selection and stopping in voluntary action: A meta-analysis and combined fMRI study

NeuroImage, 2014

Voluntary action control requires selection of appropriate responses and stopping of inappropriat... more Voluntary action control requires selection of appropriate responses and stopping of inappropriate responses. Selection and stopping are often investigated separately, but they appear to recruit similar brain regions, including the pre-supplementary motor area (preSMA) and inferior frontal gyrus. We therefore examined the evidence for overlap of selection and stopping using two approaches: a meta-analysis of existing studies of selection and stopping, and a novel within-subject fMRI study in which action selection and a stop signal task were combined factorially. The novel fMRI study also permitted us to investigate hypotheses regarding a common mechanism for selection and stopping. The preSMA was identified by both methods as common to selection and stopping. However, stopping a selected action did not recruit preSMA more than stopping a specified action, nor did stop signal reaction times differ significantly across the two conditions. These findings suggest that the preSMA supports both action selection and stopping, but the two processes may not require access to a common inhibition mechanism. Instead, the preSMA might represent information about potential actions that is used in both action selection and stopping in order to resolve conflict between competing available responses.

Research paper thumbnail of The prefrontal cortex achieves inhibitory control by facilitating subcortical motor pathway connectivity

The Journal of neuroscience : the official journal of the Society for Neuroscience, Jan 14, 2015

Communication between the prefrontal cortex and subcortical nuclei underpins the control and inhi... more Communication between the prefrontal cortex and subcortical nuclei underpins the control and inhibition of behavior. However, the interactions in such pathways remain controversial. Using a stop-signal response inhibition task and functional imaging with analysis of effective connectivity, we show that the lateral prefrontal cortex influences the strength of communication between regions in the frontostriatal motor system. We compared 20 generative models that represented alternative interactions between the inferior frontal gyrus, presupplementary motor area (preSMA), subthalamic nucleus (STN), and primary motor cortex during response inhibition. Bayesian model selection revealed that during successful response inhibition, the inferior frontal gyrus modulates an excitatory influence of the preSMA on the STN, thereby amplifying the downstream polysynaptic inhibition from the STN to the motor cortex. Critically, the strength of the interaction between preSMA and STN, and the degree o...

Research paper thumbnail of Failing to Forget: Inhibitory-Control Deficits Compromise Memory Suppression in Posttraumatic Stress Disorder.

Most people have experienced distressing events that they would rather forget. Although memories ... more Most people have experienced distressing events that they would rather forget. Although memories of such events
become less intrusive with time for the majority of people, those with posttraumatic stress disorder (PTSD) are afflicted
by vivid, recurrent memories of their trauma. Often triggered by reminders in the daily environment, these memories
can cause severe distress and impairment. We propose that difficulties with intrusive memories in PTSD arise in part
from a deficit in engaging inhibitory control to suppress episodic retrieval. We tested this hypothesis by adapting
the think/no-think paradigm to investigate voluntary memory suppression of aversive scenes cued by naturalistic
reminders. Retrieval suppression was compromised significantly in PTSD patients, compared with trauma-exposed
control participants. Furthermore, patients with the largest deficits in suppression-induced forgetting were also those
with the most severe PTSD symptoms. These results raise the possibility that prefrontal mechanisms supporting
inhibitory control over memory are impaired in PTSD.

Research paper thumbnail of Retrieval induces adaptive forgetting of competing memories via cortical pattern suppression

Remembering a past experience can, surprisingly, cause forgetting. Forgetting arises when other c... more Remembering a past experience can, surprisingly, cause forgetting. Forgetting arises when other competing traces interfere with retrieval and inhibitory control mechanisms are engaged to suppress the distraction they cause. This form of forgetting is considered to be adaptive because it reduces future interference. The effect of this proposed inhibition process on competing memories has, however, never been observed, as behavioral methods are ‘blind’ to retrieval dynamics and neuroimaging methods have not isolated retrieval of individual memories. We developed a canonical template tracking method to quantify the activation state of individual target memories and competitors during retrieval. This method revealed that repeatedly retrieving target memories suppressed cortical patterns unique to competitors. Pattern suppression was related to engagement of prefrontal regions that have been implicated in resolving retrieval competition and, critically, predicted later forgetting. Thus, our findings demonstrate a cortical pattern suppression mechanism through which remembering adaptively shapes which aspects of our past remain accessible.

Research paper thumbnail of Older Adults Can Suppress Unwanted Memories When Given an Appropriate Strategy

Memory suppression refers to the ability to exclude distracting memories from conscious awareness... more Memory suppression refers to the ability to exclude distracting memories from conscious awareness, and this ability can be assessed with the think/no-think paradigm. Recent research with older adults has provided evidence suggesting both intact and deficient memory suppression. The present studies seek to understand the conditions contributing to older adults’ ability to suppress memories voluntarily. We report 2 experiments
indicating that the specificity of the think/no-think task instructions contributes to older adults’ suppression
success: When older adults receive open-ended instructions that require them to develop a retrieval suppression
strategy on their own, they show diminished memory suppression compared with younger adults. Conversely, when older adults receive focused instructions directing them to a strategy thought to better isolate inhibitory control, they show suppression-induced forgetting similar to that exhibited by younger adults. Younger adults demonstrate memory suppression regardless of the specificity of the instructions given, suggesting that the ability to select a successful suppression strategy spontaneously may be compromised in
older adults. If so, this deficit may be associated with diminished control over unwanted memories in naturalistic settings if impeded strategy development reduces the successful deployment of inhibitory control.

Research paper thumbnail of The Prefrontal Cortex Achieves Inhibitory Control by Facilitating Subcortical Motor Pathway Connectivity

Communication between the prefrontal cortex and subcortical nuclei underpins the control and inhi... more Communication between the prefrontal cortex and subcortical nuclei underpins the control and inhibition of behavior. However, the interactions in such pathways remain controversial. Using a stop-signal response inhibition task and functional imaging with analysis of effective connectivity, we show that the lateral prefrontal cortex influences the strength of communication between regions in the frontostriatal motor system. We compared 20 generative models that represented alternative interactions between the inferior frontal gyrus, presupplementary motor area (preSMA), subthalamic nucleus (STN), and primary motor cortex during response inhibition.
Bayesian model selection revealed that during successful response inhibition, the inferior frontal gyrus modulates an excitatory influence of the preSMA on the STN, thereby amplifying the downstream polysynaptic inhibition from the STN to the motor cortex. Critically, the strength of the interaction between preSMA and STN, and the degree of modulation by the inferior frontal gyrus, predicted individual
differences in participants’ stopping performance (stop-signal reaction time). We then used diffusion-weighted imaging with tractography to assess white matter structure in the pathways connecting these three regions. The mean diffusivity in tracts between preSMA and the STN, and between the inferior frontal gyrus and STN, also predicted individual differences in stopping efficiency. Finally, we found that white matter structure in the tract between preSMA and STN correlated with effective connectivity of the same pathway, providing important cross-modal validation of the effective connectivity measures. Together, the results demonstrate the network dynamics and
modulatory role of the prefrontal cortex that underpin individual differences in inhibitory control.

Research paper thumbnail of Adaptive Top–Down Suppression of Hippocampal Activity and the Purging of Intrusive Memories from Consciousness

When reminded of unwanted memories, people often attempt to suppress these experiences from aware... more When reminded of unwanted memories, people often
attempt to suppress these experiences from awareness. Prior
work indicates that control processes mediated by the dorsolateral prefrontal cortex (DLPFC) modulate hippocampal activity during such retrieval suppression. It remains unknown whether this modulation plays a role in purging an intrusive memory from consciousness. Here, we combined fMRI and effective connectivity analyses with phenomenological reports to scrutinize a role for adaptive top–down suppression of hippocampal retrieval processes in terminating mnemonic awareness of intrusive memories. Participants either suppressed or recalled memories of pictures depicting faces or places. After each trial, they reported their success at regulating awareness of the memory. DLPFC activation was greatest when unwanted memories intruded into consciousness and needed to be purged, and this increased engagement predicted superior control of intrusive memories over time. However, hippocampal activity was decreased during the suppression
of place memories only. Importantly, the inhibitory
influence of the DLPFC on the hippocampus was linked to the
ensuing reduction in intrusions of the suppressed memories.
Individuals who exhibited negative top–down coupling during
early suppression attempts experienced fewer involuntary memory intrusions later on. Over repeated suppressions, the DLPFC–hippocampus connectivity grew less negative with the degree that they no longer had to purge unwanted memories from awareness. These findings support a role of DLPFC in countermanding the unfolding recollection of an unwanted memory
via the suppression of hippocampal processing, a mechanism
that may contribute to adaptation in the aftermath of traumatic
experiences.

Research paper thumbnail of The origins of repetitive thought in rumination: Separating cognitive style from deficits in inhibitory control over memory

Background and objectives: Rumination is a major contributor to the maintenance of affective diso... more Background and objectives: Rumination is a major contributor to the maintenance of affective disorders
and has been linked to memory control deficits. However, ruminators often report intentionally engaging
in repetitive thought due to its perceived benefits. Deliberate re-processing may lead to the appearance
of a memory control deficit that is better explained as a difference in cognitive style.
Methods: Ninety-six undergraduate students volunteered to take part in a direct-suppression variant of
the Think/No-Think paradigm after which they completed self-report measures of rumination and the
degree to which they deliberately re-processed the to-be-suppressed items.
Results: We demonstrate a relation between rumination and impaired suppression-induced forgetting.
This relation is robust even when controlling for deliberate re-processing of the to-be-suppressed items,
a behavior itself related to both rumination and suppression. Therefore, whereas conscious fixation on
to-be-suppressed items reduced memory suppression, it did not fully account for the relation between
rumination and memory suppression.
Limitations: The current experiment employed a retrospective measure of deliberate re-processing in the
context of an unscreened university sample; future research might therefore generalize our findings
using an online measure of deliberate re-processing or within a clinical population.
Conclusions: We provide evidence that deliberate re-processing accounts for some e but not all e of the
relation between rumination and suppression-induced forgetting. The present findings, observed in a
paradigm known to engage top-down inhibitory modulation of mnemonic processing, provide the most
theoretically focused evidence to date for the existence of a memory control deficit in rumination.

Research paper thumbnail of Examining the costs and benefits of inhibition in memory retrieval

Inhibitory control is thought to serve an adaptive function in controlling behavior, with individ... more Inhibitory control is thought to serve an adaptive function in controlling behavior, with individual differences predicting variation in numerous cognitive functions. However, inhibition is more properly construed as inducing both benefits and costs to performance. Benefits arise at the point when inhibition prevents expression of an unwanted or contextually inappropriate response; costs arise later, when access to the inhibited representation is
required by other processes. Here we illustrate how failure to consider both the costs and benefits of inhibition has generated confusion in the literature on individual differences
in cognitive control. Using retrieval-induced forgetting as a model case, we illustrate this by showing that changing the way that retrieval-induced forgetting is measured to allow greater expression of the benefits of inhibition together with the costs can reduce and even reverse the theoretically predicted correlation between motor and memory inhibition. Specifically, we show that when the final test in a retrieval-induced forgetting procedure employs item-specific cues (i.e., category-plus-stem cued recall and item-recognition) that better isolate the lingering costs of inhibition, better motor response inhibition (faster stop-signal reaction times) predicts greater retrieval-induced forgetting. In striking contrast, when the final test is less well controlled, allowing both the costs and benefits of inhibition to contribute, motor response inhibition has the opposite relationship with retrieval-induced forgetting. These findings underscore the importance of considering the correlated costs and benefits problem when studying individual differences in inhibitory control. More generally, they suggest that a shared inhibition mechanism may underlie
people’s ability to control memories and actions.

Research paper thumbnail of Direct suppression as a mechanism for controlling unpleasant memories in daily life

Suppressing unwanted memories can impair their later recall. Recent work shows that this forgetti... more Suppressing unwanted memories can impair their later recall. Recent work shows that this forgetting is achieved by at least two mechanisms supported by distinct neural systems: thought substitution and direct suppression (Benoit & Anderson, 2012). Here, we examined whether direct suppression, thought to be
achieved by down-regulation of hippocampal activity, can disrupt memory of aversive scenes, and, if so,whether this disruption is linked to people’s perception of their ability to control intrusive thoughts. We presented participants with strong naturalistic reminders to aversive scenes and asked them to either
covertly retrieve or directly suppress the associated scenes. Later, participants were cued with the reminders and asked to recall the scenes in detail. Direct suppression reduced recall probability of the
scenes and also reduced the number of details recalled, even when scenes were remembered. Deficits in recall arose for minor details but also for details central to each scene’s gist. Participants with higher self-perceived control abilities over intrusive thoughts showed greater forgetting than did those reporting lower levels of control. These findings suggest that inhibitory processes underlying direct suppression can disrupt retention of aversive visual memories and link those processes to individual differences in
control over intrusive thoughts in everyday life. These findings reinforce the possibility that inhibition may be less efficient in people likely to acquire posttraumatic stress disorder in the wake of a traumatic experience.

Research paper thumbnail of Neural mechanisms of Motivated Forgetting

Not all memories are equally welcome in awareness. People limit the time they spend thinking abo... more Not all memories are equally welcome in awareness.
People limit the time they spend thinking about unpleasant
experiences, a process that begins during encoding,
but that continues when cues later remind someone of
the memory. Here, we review the emerging behavioural
and neuroimaging evidence that suppressing awareness
of an unwelcome memory, at encoding or retrieval, is
achieved by inhibitory control processes mediated by
the lateral prefrontal cortex. These mechanisms interact
with neural structures that represent experiences in
memory, disrupting traces that support retention. Thus,
mechanisms engaged to regulate momentary awareness
introduce lasting biases in which experiences remain
accessible. We argue that theories of forgetting
that neglect the motivated control of awareness omit a
powerful force shaping the retention of our past.

Research paper thumbnail of Suppressing unwanted memories reduces their unconscious influence via targeted cortical inhibition

Suppressing retrieval of unwanted memories reduces their later conscious recall. It is widely be... more Suppressing retrieval of unwanted memories reduces their later
conscious recall. It is widely believed, however, that suppressed
memories can continue to exert strong unconscious effects that
may compromise mental health. Here we show that excluding
memories from awareness not only modulates medial temporal
lobe regions involved in explicit retention, but also neocortical
areas underlying unconscious expressions of memory. Using
repetition priming in visual perception as a model task, we found
that excluding memories of visual objects from consciousness
reduced their later indirect influence on perception, literally making
the content of suppressed memories harder for participants to
see. Critically, effective connectivity and pattern similarity analysis
revealed that suppression mechanisms mediated by the right
middle frontal gyrus reduced activity in neocortical areas involved
in perceiving objects and targeted the neural populations most
activated by reminders. The degree of inhibitory modulation of
the visual cortex while people were suppressing visual memories
predicted, in a later perception test, the disruption in the neural
markers of sensory memory. These findings suggest a neurobiological model of how motivated forgetting affects the unconscious expression of memory that may be generalized to other types of memory content. More generally, they suggest that the century old assumption that suppression leaves unconscious memories intact should be reconsidered.

Research paper thumbnail of Suppressing unwanted memories by executive control

Freud proposed that unwanted memories can be forgotten by pushing them into the unconscious, a pr... more Freud proposed that unwanted memories can be forgotten by pushing them into the unconscious, a process called repression1. The existence of repression has remained controversial for more than a century, in part because of its strong coupling with trauma, and the ethical and practical difficulties of studying such processes in controlled experiments. However, behavioural and neurobiological research on memory and attention shows that people have executive control processes directed at minimizing perceptual distraction2, 3, overcoming interference during short and long-term memory tasks3, 4, 5, 6, 7 and stopping strong habitual responses to stimuli8, 9, 10, 11, 12, 13. Here we show that these mechanisms can be recruited to prevent unwanted declarative memories from entering awareness, and that this cognitive act has enduring consequences for the rejected memories. When people encounter cues that remind them of an unwanted memory and they consistently try to prevent awareness of it, the later recall of the rejected memory becomes more difficult. The forgetting increases with the number of times the memory is avoided, resists incentives for accurate recall and is caused by processes that suppress the memory itself. These results show that executive control processes not uniquely tied to trauma may provide a viable model for repression.

Research paper thumbnail of Neural systems underlying the suppression of unwanted memories

Over a century ago, Freud proposed that unwanted memories can be excluded from awareness, a proc... more Over a century ago, Freud proposed that unwanted memories can be excluded
from awareness, a process called repression. It is unknown, however, how
repression occurs in the brain. We used functional magnetic resonance imaging
to identify the neural systems involved in keeping unwanted memories out of
awareness. Controlling unwanted memories was associated with increased
dorsolateral prefrontal activation, reduced hippocampal activation, and impaired
retention of those memories. Both prefrontal cortical and right hippocampal
activations predicted the magnitude of forgetting. These results
confirm the existence of an active forgetting process and establish a neurobiological
model for guiding inquiry into motivated forgetting.

Research paper thumbnail of Opposing mechanisms support the voluntary forgetting of unwanted memories

Reminders of the past can trigger the recollection of events that one would rather forget. Here,... more Reminders of the past can trigger the recollection of
events that one would rather forget. Here, using
fMRI, we demonstrate two distinct neural mechanisms
that foster the intentional forgetting of such
unwanted memories. Both mechanisms impair
long-term retention by limiting momentary awareness
of the memories, yet they operate in opposite
ways. One mechanism, direct suppression, disengages
episodic retrieval through the systemic inhibition
of hippocampal processing that originates
from right dorsolateral prefrontal cortex (PFC). The
opposite mechanism, thought substitution, instead
engages retrieval processes to occupy the limited
focus of awareness with a substitute memory. It is
mediated by interactions between left caudal and
midventrolateral PFC that support the selective
retrieval of substitutes in the context of prepotent,
unwanted memories. These findings suggest that
we are not at the mercy of passive forgetting; rather,
our memories can be shaped by two opposite mechanisms
of mnemonic control.