Reducing future fears by suppressing the brain mechanisms underlying episodic simulation

Significance Humans possess the remarkable ability to recombine details of divergent memories into imaginings of future events. Such imaginings are useful, for example, because they foster planning and motivate farsighted decisions. Importantly, recurrently imagining feared situations can also undermine our well-being and may even contribute to the development of anxiety. Here, we demonstrate that fearful imaginings about the future can be inhibited by neural mechanisms that help to suppress the past. Importantly, suppression reduces later apprehensiveness about the feared events, a benefit that was diminished in individuals with greater trait anxiety. This pattern suggests that the observed inhibition mechanism serves to control people’s future fears and its disruption may foster psychological disorders characterized by intrusive prospective thoughts. Imagining future events conveys adaptive benefits, yet recurrent simulations of feared situations may help to maintain anxiety. In two studies, we tested the hypothesis that people can attenuate future fears by suppressing anticipatory simulations of dreaded events. Participants repeatedly imagined upsetting episodes that they feared might happen to them and suppressed imaginings of other such events. Suppressing imagination engaged the right dorsolateral prefrontal cortex, which modulated activation in the hippocampus and in the ventromedial prefrontal cortex (vmPFC). Consistent with the role of the vmPFC in providing access to details that are typical for an event, stronger inhibition of this region was associated with greater forgetting of such details. Suppression further hindered participants’ ability to later freely envision suppressed episodes. Critically, it also reduced feelings of apprehensiveness about the feared scenario, and individuals who were particularly successful at down-regulating fears were also less trait-anxious. Attenuating apprehensiveness by suppressing simulations of feared events may thus be an effective coping strategy, suggesting that a deficiency in this mechanism could contribute to the development of anxiety.

[1]  K. Ochsner,et al.  Sadness Shifts to Anxiety Over Time and Distance From the National Tragedy in Newtown, Connecticut , 2015, Psychological science.

[2]  Michael C. Anderson,et al.  Neural mechanisms of motivated forgetting , 2014, Trends in Cognitive Sciences.

[3]  Jennifer A. Silvers,et al.  Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. , 2014, Cerebral cortex.

[4]  Joseph M. Orr,et al.  The Organization of Right Prefrontal Networks Reveals Common Mechanisms of Inhibitory Regulation Across Cognitive, Emotional, and Motor Processes. , 2016, Cerebral cortex.

[5]  Sang Hee Kim,et al.  Neural Correlates of Positive and Negative Emotion Regulation , 2007, Journal of Cognitive Neuroscience.

[6]  S. H. Hulse,et al.  Amount and percentage of reinforcement and duration of goal confinement in conditioning and extinction. , 1958, Journal of experimental psychology.

[7]  P. Hertel,et al.  Depressive Deficits in Forgetting , 2003, Psychological science.

[8]  R. Henson,et al.  How schema and novelty augment memory formation , 2012, Trends in Neurosciences.

[9]  D. Hassabis,et al.  Deconstructing episodic memory with construction , 2007, Trends in Cognitive Sciences.

[10]  D. Hassabis,et al.  Patients with hippocampal amnesia cannot imagine new experiences , 2007, Proceedings of the National Academy of Sciences.

[11]  Karl J. Friston,et al.  Comparing Families of Dynamic Causal Models , 2010, PLoS Comput. Biol..

[12]  A. D'Argembeau On the Role of the Ventromedial Prefrontal Cortex in Self-Processing: The Valuation Hypothesis , 2013, Front. Hum. Neurosci..

[13]  D. Shohamy,et al.  Ventromedial prefrontal-subcortical systems and the generation of affective meaning , 2012, Trends in Cognitive Sciences.

[14]  Daniel L Schacter,et al.  Ventromedial prefrontal cortex supports affective future simulation by integrating distributed knowledge , 2014, Proceedings of the National Academy of Sciences.

[15]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[16]  M. Eysenck,et al.  Anxiety and cognitive performance: attentional control theory. , 2007, Emotion.

[17]  A. Wells A cognitive model of social phobia , 1995 .

[18]  Arnaud D'Argembeau,et al.  Networks of prospective thoughts: The organisational role of emotion and its impact on well-being , 2016, Cognition & emotion.

[19]  Guillaume A. Rousselet,et al.  Robust Correlation Analyses: False Positive and Power Validation Using a New Open Source Matlab Toolbox , 2012, Front. Psychology.

[20]  Margaret L. Schlichting,et al.  Hippocampal–medial prefrontal circuit supports memory updating during learning and post-encoding rest , 2016, Neurobiology of Learning and Memory.

[21]  T. Borkovec,et al.  The role of worrisome thinking in the suppression of cardiovascular response to phobic imagery. , 1993, Behaviour research and therapy.

[22]  Mauricio R. Delgado,et al.  Overlapping neural systems mediating extinction, reversal and regulation of fear , 2010, Trends in Cognitive Sciences.

[23]  Timothy E. J. Behrens,et al.  Online evaluation of novel choices by simultaneous representation of multiple memories , 2013, Nature Neuroscience.

[24]  M. Linden,et al.  Frequency, characteristics and functions of future‐oriented thoughts in daily life , 2011 .

[25]  Alana T. Wong,et al.  Age-Related Changes in the Episodic Simulation of Future Events , 2008, Psychological science.

[26]  D. Gilbert,et al.  A Wandering Mind Is an Unhappy Mind , 2010, Science.

[27]  Sonia J. Bishop,et al.  Unraveling the Anxious Mind: Anxiety, Worry, and Frontal Engagement in Sustained Attention Versus Off-Task Processing , 2013, Cerebral cortex.

[28]  Guy M. Goodwin,et al.  Mood stability versus mood instability in bipolar disorder: A possible role for emotional mental imagery , 2011, Behaviour research and therapy.

[29]  M. Eysenck,et al.  Anxiety, inhibition, efficiency, and effectiveness. An investigation using antisaccade task. , 2009, Experimental psychology.

[30]  Michael C. Anderson,et al.  Suppressing unwanted memories reduces their unconscious influence via targeted cortical inhibition , 2014, Proceedings of the National Academy of Sciences.

[31]  D. Schacter,et al.  Episodic future thinking in generalized anxiety disorder. , 2015, Journal of anxiety disorders.

[32]  S. Righi,et al.  Emotions shape memory suppression in trait anxiety , 2014, Front. Psychol..

[33]  T. Curran,et al.  Prefrontal Regions Orchestrate Suppression of Emotional Memories via a Two-Phase Process , 2007, Science.

[34]  Michael C. Anderson,et al.  Direct Suppression as a Mechanism for Controlling Unpleasant Memories in Daily Life , 2014, Journal of experimental psychology. General.

[35]  André Aleman,et al.  The neural correlates of worry in association with individual differences in neuroticism , 2014, Human brain mapping.

[36]  Brice A. Kuhl,et al.  Predicting the integration of overlapping memories by decoding mnemonic processing states during learning , 2016, NeuroImage.

[37]  Shelley E. Taylor,et al.  The Effects of Mental Simulation on Coping with Controllable Stressful Events , 1999 .

[38]  E. Holmes,et al.  Prospective mental imagery in patients with major depressive disorder or anxiety disorders , 2011, Journal of anxiety disorders.

[39]  Karl J. Friston,et al.  Ten simple rules for dynamic causal modeling , 2010, NeuroImage.

[40]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[41]  Michael C. Anderson,et al.  Inducing amnesia through systemic suppression , 2016, Nature Communications.

[42]  Michael C. Anderson,et al.  Interference and inhibition in memory retrieval. , 1996 .

[43]  Timothy D. Wilson,et al.  Prospection: Experiencing the Future , 2007, Science.

[44]  A. Hackmann,et al.  Intrusive imagery in severe health anxiety: Prevalence, nature and links with memories and maintenance cycles , 2010, Behaviour research and therapy.

[45]  Quincy J. J. Wong,et al.  Impact of anticipatory processing versus distraction on multiple indices of anxiety in socially anxious individuals. , 2011, Behaviour research and therapy.

[46]  Michael C. Anderson,et al.  Strength of Coupling within a Mnemonic Control Network Differentiates Those Who Can and Cannot Suppress Memory Retrieval , 2013, The Journal of Neuroscience.

[47]  Brice A. Kuhl,et al.  Neural Systems Underlying the Suppression of Unwanted Memories , 2004, Science.

[48]  W. M. Cox,et al.  Dimensions of Thought Flow in Everyday Life , 1987 .

[49]  Michael C. Anderson,et al.  Opposing Mechanisms Support the Voluntary Forgetting of Unwanted Memories , 2012, Neuron.

[50]  Dagmar Zeithamova,et al.  Hippocampal and Ventral Medial Prefrontal Activation during Retrieval-Mediated Learning Supports Novel Inference , 2012, Neuron.

[51]  R. N. Spreng,et al.  The Future of Memory: Remembering, Imagining, and the Brain , 2012, Neuron.

[52]  L. Jason,et al.  Time Orientation: Past, Present, and Future Perceptions , 1989 .

[53]  P. Lewis,et al.  Overlapping memory replay during sleep builds cognitive schemata , 2011, Trends in Cognitive Sciences.

[54]  Michael C. Anderson,et al.  Suppressing unwanted memories by executive control , 2001, Nature.

[55]  Michael C. Anderson,et al.  Adaptive Top–Down Suppression of Hippocampal Activity and the Purging of Intrusive Memories from Consciousness , 2015, Journal of Cognitive Neuroscience.

[56]  Daniel L Schacter,et al.  Worrying about the future: An episodic specificity induction impacts problem solving, reappraisal, and well-being. , 2016, Journal of experimental psychology. General.

[57]  Michael C. Anderson,et al.  Failing to Forget: Inhibitory Control Deficits Compromise Memory Suppression in Posttraumatic Stress Dis... , 2015 .

[58]  Zara M. Bergström,et al.  ERP and behavioural evidence for direct suppression of unwanted memories , 2009, NeuroImage.

[59]  S. Bishop Trait anxiety and impoverished prefrontal control of attention , 2009, Nature Neuroscience.

[60]  Jonathan Smallwood,et al.  Thinking too much: self-generated thought as the engine of neuroticism , 2015, Trends in Cognitive Sciences.

[61]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[62]  I. Gotlib,et al.  Remembering the good, forgetting the bad: intentional forgetting of emotional material in depression. , 2005, Journal of abnormal psychology.

[63]  Tim Curran,et al.  Suppression of Emotional and Nonemotional Content in Memory , 2006, Psychological science.

[64]  D. Schacter,et al.  Characterizing Age-related Changes in Remembering the past and Imagining the Future Experiment 1 , 2022 .

[65]  Kristin N. Mauldin,et al.  Role of the hippocampus in remembering the past and imagining the future , 2010, Proceedings of the National Academy of Sciences.

[66]  E Fox,et al.  Attentional bias in anxiety: selective or not? , 1993, Behaviour research and therapy.

[67]  E. Fox,et al.  Attentional Control and Suppressing Negative Thought Intrusions in Pathological Worry , 2015, Clinical psychological science : a journal of the Association for Psychological Science.

[68]  R. Benoit,et al.  A Neural Mechanism Mediating the Impact of Episodic Prospection on Farsighted Decisions , 2011, The Journal of Neuroscience.

[69]  B. Harrison,et al.  Neural signatures of human fear conditioning: an updated and extended meta-analysis of fMRI studies , 2016, Molecular Psychiatry.

[70]  Francesc Colom,et al.  Mental imagery as an emotional amplifier: application to bipolar disorder. , 2008, Behaviour research and therapy.

[71]  G. Winocur,et al.  Aging and autobiographical memory: dissociating episodic from semantic retrieval. , 2002, Psychology and aging.

[72]  Michael C. Anderson,et al.  The origins of repetitive thought in rumination: Separating cognitive style from deficits in inhibitory control over memory , 2015, Journal of behavior therapy and experimental psychiatry.

[73]  Saima Noreen,et al.  It's all in the detail: intentional forgetting of autobiographical memories using the autobiographical think/no-think task. , 2013, Journal of experimental psychology. Learning, memory, and cognition.

[74]  A. MacLeod,et al.  Worry and the Simulation of Future Outcomes , 2002 .

[75]  P. Boyer Evolutionary economics of mental time travel? , 2008, Trends in Cognitive Sciences.

[76]  A. MacLeod,et al.  Anxiety, depression, and the anticipation of future positive and negative experiences. , 1996, Journal of abnormal psychology.

[77]  Y. Trope,et al.  Construal-level theory of psychological distance. , 2010, Psychological review.

[78]  Mieke Verfaellie,et al.  Medial Temporal Lobe Damage Causes Deficits in Episodic Memory and Episodic Future Thinking Not Attributable to Deficits in Narrative Construction , 2011, The Journal of Neuroscience.

[79]  M. Koenigs,et al.  Functional anatomy of ventromedial prefrontal cortex: implications for mood and anxiety disorders , 2012, Molecular Psychiatry.

[80]  Andrew Mathews,et al.  Mental imagery in emotion and emotional disorders. , 2010, Clinical psychology review.

[81]  Jutta Joormann,et al.  Training forgetting of negative material in depression. , 2009, Journal of abnormal psychology.

[82]  Daniel Kahneman,et al.  Availability: A heuristic for judging frequency and probability , 1973 .

[83]  Michael C. Anderson,et al.  Prefrontal–hippocampal pathways underlying inhibitory control over memory , 2016, Neurobiology of Learning and Memory.

[84]  William W Eaton,et al.  Anxiety and depressive disorders and the five‐factor model of personality: A higher‐ and lower‐order personality trait investigation in a community sample , 2004, Depression and anxiety.

[85]  A. Mecklinger,et al.  Trait anxiety, working memory capacity, and the effectiveness of memory suppression. , 2011, Scandinavian journal of psychology.

[86]  D. Schacter,et al.  Specifying the core network supporting episodic simulation and episodic memory by activation likelihood estimation , 2015, Neuropsychologia.

[87]  T. Suddendorf,et al.  The future is here: A review of foresight systems in anxiety and depression , 2014, Cognition & emotion.

[88]  B. Doré,et al.  Sadness shifts to anxiety with time and distance from national tragedy in Newtown CT , 2014 .

[89]  R. Cialdini,et al.  Self-Relevant Scenarios as Mediators of Likelihood Estimates and Compliance: Does Imagining Make It So? , 1982 .