Computerized Exposure Therapy for Spider Phobia: Effects of Cardiac Timing and Interoceptive Ability on Subjective and Behavioral Outcomes

Objective Spider phobia is a common form of anxiety disorder for which exposure therapy is an effective first-line treatment. Motivated by the observed modulation of threat processing by afferent cardiac signals, we tested the hypothesis that interoceptive information concerning cardiovascular arousal can influence the outcomes of computerized exposure therapy for spider phobia. Method Fifty-three normal healthy participants with high spider phobia scores underwent one of the following three modified computerized exposure protocols, defined by the timing of exposure to brief spider stimuli within the cardiac cycle: systole (during afferent baroreceptor firing); diastole (during baroreceptor-quiescent interbeat interval); random (noncontingent on cardiac cycle). Outcomes were judged on phobic and anxiety measures and physiological data (skin conductance). Individuals were also rated on interoceptive accuracy. Results MANCOVA analysis showed that timing group affected the outcome measures (F(10,80) = 2.405, p = .015) and there was a group interaction with interoception ability (F(15,110) = 1.808, p = .045). Subjective symptom reduction was greatest in the systolic group relative to the other two groups (diastolic (t = 3.115, ptukey = .009); random (t = 2.438, ptukey = .048)), with greatest reductions in those participants with lower interoceptive accuracy. Behavioral aversion reduced more in cardiac-contingent groups than the noncontingent (random) group (diastolic (t = 3.295, ptukey = .005); systolic (t = 2.602, ptukey = .032)). Physiological (skin conductance response) responses remained strongest for spider stimuli presented at cardiac systole. Conclusions Interoceptive information influences exposure benefit. The reduction in the subjective expression of fear/phobia is facilitated by “bottom-up” afferent signals, whereas improvement in the behavioral expression is further dependent on “top-down” representation of self-related physiology (heart rhythm). Individual interoceptive differences moderate these effects, suggesting means to personalize therapy.

[1]  C. Ring,et al.  Effects of arterial and cardiopulmonary baroreceptor activation on the upper limb nociceptive flexion reflex and electrocutaneous pain in humans , 2008, PAIN®.

[2]  H. Critchley,et al.  Emotional regulation and bodily sensation: interoceptive awareness is intact in borderline personality disorder. , 2013, Journal of personality disorders.

[3]  P. Lang,et al.  Psychometric description of some specific-fear questionnaires. , 1974 .

[4]  C. Ring,et al.  The human nociceptive flexion reflex threshold is higher during systole than diastole. , 2002, Psychophysiology.

[5]  A. Craig.  How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[6]  Andrea Desantis,et al.  Attenuation of auditory N1 results from identity‐specific action‐effect prediction , 2013, The European journal of neuroscience.

[7]  E. Schröger,et al.  Attenuated human auditory middle latency response and evoked 40‐Hz response to self‐initiated sounds , 2009, The European journal of neuroscience.

[8]  M. Bradley,et al.  Remembering pictures: pleasure and arousal in memory. , 1992, Journal of experimental psychology. Learning, memory, and cognition.

[9]  H. Critchley,et al.  Knowing your own heart: Distinguishing interoceptive accuracy from interoceptive awareness , 2015, Biological Psychology.

[10]  F. Goodwin,et al.  The de facto US mental and addictive disorders service system. Epidemiologic catchment area prospective 1-year prevalence rates of disorders and services. , 1993, Archives of general psychiatry.

[11]  K. Domschke,et al.  Interoceptive sensitivity in anxiety and anxiety disorders: an overview and integration of neurobiological findings. , 2010, Clinical psychology review.

[12]  H. Critchley,et al.  Visceral Influences on Brain and Behavior , 2013, Neuron.

[13]  Cristina M. Alberini,et al.  Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes? , 2005, Trends in Neurosciences.

[14]  H. Critchley,et al.  Fear from the Heart: Sensitivity to Fear Stimuli Depends on Individual Heartbeats , 2014, The Journal of Neuroscience.

[15]  Mary Helen Immordino‐Yang,et al.  The Brainstem in Emotion: A Review , 2017, Front. Neuroanat..

[16]  O. Van den Bergh,et al.  Interoception and symptom reporting: disentangling accuracy and bias , 2015, Front. Psychol..

[17]  H. Critchley,et al.  Threat and the Body: How the Heart Supports Fear Processing , 2016, Trends in Cognitive Sciences.

[18]  Lars-Göran Öst,et al.  One-session therapist directed exposure vs two forms of manual directed self-exposure in the treatment of spider phobia. , 1995, Behaviour research and therapy.

[19]  A. Wells,et al.  Social phobic interoception: effects of bodily information on anxiety, beliefs and self-processing. , 2001, Behaviour research and therapy.

[20]  Woong Sun,et al.  Amygdala depotentiation and fear extinction , 2007, Proceedings of the National Academy of Sciences.

[21]  S. Blakemore,et al.  The perception of self-produced sensory stimuli in patients with auditory hallucinations and passivity experiences: evidence for a breakdown in self-monitoring , 2000, Psychological Medicine.

[22]  F. Watts,et al.  Questionnaire dimensions of spider phobia. , 1984, Behaviour research and therapy.

[23]  Hugo D. Critchley,et al.  Interactions between visceral afferent signaling and stimulus processing , 2015, Front. Neurosci..

[24]  S. Garfinkel,et al.  Impaired Contextual Modulation of Memories in PTSD: An fMRI and Psychophysiological Study of Extinction Retention and Fear Renewal , 2014, The Journal of Neuroscience.

[25]  K. Nader,et al.  Enhancement of fear memory by retrieval through reconsolidation , 2014, eLife.

[26]  H. Critchley,et al.  What the heart forgets: Cardiac timing influences memory for words and is modulated by metacognition and interoceptive sensitivity. , 2013, Psychophysiology.

[27]  S. Schulz,et al.  Enhanced cardiac perception predicts impaired performance in the Iowa Gambling Task in patients with panic disorder , 2014, Brain and behavior.

[28]  R. Kessler,et al.  The cross-national epidemiology of specific phobia in the World Mental Health Surveys , 2017, Psychological Medicine.

[29]  Stella Li,et al.  Estradiol is associated with altered cognitive and physiological responses during fear conditioning and extinction in healthy and spider phobic women. , 2016, Behavioral neuroscience.

[30]  R. Schandry,et al.  Heart beat perception and emotional experience. , 1981, Psychophysiology.

[31]  I. Izquierdo,et al.  Treatment of fear memories: interactions between extinction and reconsolidation. , 2011, Anais da Academia Brasileira de Ciencias.

[32]  R. Schandry,et al.  Enhanced cardiac perception is associated with benefits in decision-making. , 2009, Psychophysiology.

[33]  M. Bradley,et al.  Emotion, Motivation, and Anxiety: Brain Mechanisms and Psychophysiology the Motivational Organization of Emotion Patterns of Human Emotion Emotion and Perception the Psychophysiology of Picture Processing Neural Imaging: Motivation in the Visual Cortex Motivational Circuits in the Brain , 2022 .

[34]  M. Paulus,et al.  Interoception in anxiety and depression , 2010, Brain Structure and Function.

[35]  S. Umeda,et al.  How does interoceptive awareness interact with the subjective experience of emotion? An fMRI Study , 2011, Human brain mapping.

[36]  J Szymanski,et al.  Fear of Spiders Questionnaire. , 1995, Journal of behavior therapy and experimental psychiatry.

[37]  Jonathan L. C. Lee,et al.  Memory reconsolidation mediates the strengthening of memories by additional learning , 2008, Nature Neuroscience.

[38]  H. Critchley,et al.  Cognitive functioning in orthostatic hypotension due to pure autonomic failure , 2006, Clinical Autonomic Research.

[39]  Bodily arousal differentially impacts stimulus processing and memory: Norepinephrine in interoception , 2016, Behavioral and Brain Sciences.

[40]  C. Tallon-Baudry,et al.  The neural subjective frame: from bodily signals to perceptual consciousness , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  C. Ring,et al.  Towards a psychophysics of interoceptive processes: the measurement of heartbeat detection , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[42]  Kevin M. Connolly,et al.  The Disgust Propensity and Sensitivity Scale-Revised: psychometric properties and specificity in relation to anxiety disorder symptoms. , 2007, Journal of anxiety disorders.

[43]  R. Carleton,et al.  "But it might be a heart attack": intolerance of uncertainty and panic disorder symptoms. , 2014, Journal of anxiety disorders.

[44]  B. Wallin,et al.  Muscle sympathetic response to arousal predicts neurovascular reactivity during mental stress , 2012, The Journal of physiology.

[45]  O. Blanke,et al.  The Insula Mediates Access to Awareness of Visual Stimuli Presented Synchronously to the Heartbeat , 2016, The Journal of Neuroscience.

[46]  L. Weiskrantz,et al.  Residual tactile sensitivity with self-directed stimulation in hemianaesthesia. , 1987, Journal of neurology, neurosurgery, and psychiatry.

[47]  B C Lacey,et al.  Two-way communication between the heart and the brain. Significance of time within the cardiac cycle. , 1978, The American psychologist.

[48]  M. Craske,et al.  First-line Treatment : a Critical Appraisal of Cognitive Behavioral Therapy Developments and Alternatives Cognitive Behavioral Therapy Anxiety Disorders Exposure Mindfulness Efficacy , 2022 .

[49]  R. Hodgson,et al.  I. Synchrony and desynchrony in fear and avoidance. , 1974, Behaviour research and therapy.

[50]  Hugo D. Critchley,et al.  Following One's Heart: Cardiac Rhythms Gate Central Initiation of Sympathetic Reflexes , 2009, The Journal of Neuroscience.

[51]  Kevin Murphy,et al.  Anatomical and functional overlap within the insula and anterior cingulate cortex during interoception and phobic symptom provocation , 2013, Human brain mapping.

[52]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[53]  D. Mcintyre,et al.  Sensory detection thresholds are modulated across the cardiac cycle: evidence that cutaneous sensibility is greatest for systolic stimulation. , 2009, Psychophysiology.

[54]  Ken A. Paller,et al.  Exposure therapy triggers lasting reorganization of neural fear processing , 2012, Proceedings of the National Academy of Sciences.

[55]  H. Critchley,et al.  Vagus Nerve Stimulation for Treatment-Resistant Depression: Behavioral and Neural Effects on Encoding Negative Material , 2007, Psychosomatic medicine.

[56]  Dan J Stein,et al.  Meta‐analysis of functional brain imaging in specific phobia , 2013, Psychiatry and clinical neurosciences.

[57]  H. Critchley,et al.  Emotional appraisal is influenced by cardiac afferent information. , 2012, Emotion.

[58]  H. Merckelbach,et al.  A comparison of two spider fear questionnaires. , 1996, Journal of behavior therapy and experimental psychiatry.

[59]  O. Blanke,et al.  Suppression of the auditory N1-component for heartbeat-related sounds reflects interoceptive predictive coding , 2014, Biological Psychology.

[60]  Karim Nader,et al.  Memory traces unbound , 2003, Trends in Neurosciences.

[61]  Bram Vervliet,et al.  Maximizing exposure therapy An inhibitory learning approach , 2015 .

[62]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[63]  T. Blumenthal,et al.  Cardiac modulation of startle eye blink. , 2009, Psychophysiology.

[64]  Y. Dudai,et al.  Stability of Retrieved Memory: Inverse Correlation with Trace Dominance , 2003, Science.

[65]  Hugo D. Critchley,et al.  Interoceptive dimensions across cardiac and respiratory axes , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[66]  D. Paré,et al.  Erasing Fear Memories with Extinction Training , 2010, The Journal of Neuroscience.

[67]  R. Rescorla.  Retraining of extinguished Pavlovian stimuli. , 2001, Journal of experimental psychology. Animal behavior processes.

[68]  D M Wolpert,et al.  Predicting the Consequences of Our Own Actions: The Role of Sensorimotor Context Estimation , 1998, The Journal of Neuroscience.

[69]  M. Bradley,et al.  Emotion and motivation II: sex differences in picture processing. , 2001, Emotion.

[70]  Lisa M. McTeague,et al.  Defensive Mobilization in Specific Phobia: Fear Specificity, Negative Affectivity, and Diagnostic Prominence , 2012, Biological Psychiatry.

[71]  S. Schütz-Bosbach,et al.  Reliability of sensory predictions determines the experience of self-agency , 2012, Behavioural Brain Research.

[72]  Sarah N Garfinkel,et al.  Interoception, emotion and brain: new insights link internal physiology to social behaviour. Commentary on:: "Anterior insular cortex mediates bodily sensibility and social anxiety" by Terasawa et al. (2012). , 2013, Social cognitive and affective neuroscience.

[73]  Olga V. Demler,et al.  Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. , 2005, Archives of general psychiatry.

[74]  B. Cuthbert,et al.  Fear and the startle reflex: blink modulation and autonomic response patterns in animal and mutilation fearful subjects. , 1997, Psychophysiology.

[75]  M. Benedek,et al.  A continuous measure of phasic electrodermal activity , 2010, Journal of Neuroscience Methods.

[76]  A. Seth.  Interoceptive inference, emotion, and the embodied self , 2013, Trends in Cognitive Sciences.

[77]  B. Teachman,et al.  Automatic processing in spider phobia: implicit fear associations over the course of treatment. , 2003, Journal of abnormal psychology.

[78]  M. Olfson,et al.  Quality of life following remission of mental disorders: findings from the National Epidemiologic Survey on Alcohol and Related Conditions. , 2013, The Journal of clinical psychiatry.

[79]  Karl J. Friston,et al.  Active interoceptive inference and the emotional brain , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[80]  I. Izquierdo,et al.  Retrieval induces reconsolidation of fear extinction memory , 2010, Proceedings of the National Academy of Sciences.

[81]  S. Mineka,et al.  Context-specificity of relapse: effects of therapist and environmental context on return of fear. , 1999, Behaviour research and therapy.