Abstract
Cognitive behavioral models of panic disorder (PD) stress the importance of an increased attentional focus towards bodily symptoms in the onset and maintenance of this debilitating anxiety disorder. In this fMRI mental tracking paradigm, we looked at the effects of focusing one’s attention internally (interoception) vs. externally (exteroception) in a well-studied group at risk for PD—that is anxiety-sensitive females (AS-high). We hypothesized that AS-high subjects compared to control subjects will present higher arousal and decreased valence scores during interoception and parallel higher activity in brain areas which are associated with fear and interoception. 24 healthy female students with high levels of anxiety sensitivity and 24 healthy female students with normal levels of anxiety sensitivity serving as control group were investigated by 3 T fMRI. Subjects either focused their attention on their heartbeats (internal condition) or on neutral tones (external condition). Task performance was monitored by reporting the number of heartbeats or tones after each block. State of arousal and emotional valence were also assessed. The high anxiety-sensitive group reported higher arousal scores compared to controls during the course of the experiment. Simultaneously, fMRI results indicated higher activation in anxiety-sensitive participants than in controls during interoception in a network of cortical and subcortical brain regions (thalamus, amygdala, parahippocampus) that overlaps with known fear circuitry structures. In particular, the activity of the right amygdala was up-regulated. Future prospective-longitudinal studies are needed to validate the role of the amygdala for transition to disorder. Attention to internal body functions up-regulates the activity of interoceptive and fear-relevant brain regions in anxiety-sensitive females, a high-risk group for the development of anxiety disorders.
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References
Andor T, Gerlach A, Rist F (2008) Superior perception of phasic physiological arousal and the detrimental consequences of the conviction to be aroused on worrying and metacognitions in GAD. J Abnorm Psychol 117:193–205
Benitez CI, Shea MT, Raffa S, Rende R, Dyck IR, Ramsawh HJ, Edelen MO, Keller MB (2009) Anxiety sensitivity as a predictor of the clinical course of panic disorders. A one year follow-up study. Depress Anxiety 26:335–342
Clark DM (1986) A cognitive approach to panic. Behav Res Ther 24:461–470
Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666
Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–195
Damasio AR, Grabowski TJ, Bechara A, Damasio H, Ponto LL, Parvizi J, Hichwa RD (2000) Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat Neurosci 3(10):1049–1056
Davis M, Whalen PG (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6:13–34
Domschke K, Stevens S, Pfleiderer B, Gerlach AL (2010) Interoceptive sensitivity in anxiety and anxiety disorders: an overview and integration of neurobiological findings. Clin Psych Rev 30:1–11
Dresler T, Guhn A, Tupak SV, Ehlis A-C, Herrmann MJ, Fallgatter AJ, Deckert J, Domschke K (2013) Revise the revised? New dimensions of the neuroanatomical hypothesis of panic disorder. J Neural Transm 120:3–29
Ehlers A (1995) A one-year prospective study of panic attacks: clinical course and factors associated with maintenance. J Abnorm Psychol 104:164–172
Ehlers A, Breuer P (1992) Increased cardiac awareness in panic disorder. J Abnorm Psychol 101:371–382
Ehlers A, Breuer P (1996) How good are patients with panic disorder at perceiving their heartbeats? Biol Psychol 42:165–182
Ehlers A, Breuer P, Dohn D, Fiegenbaum W (1995) Heartbeat perception and panic disorder: possible explanations for discrepant findings. Behav Res Ther 33:69–76
Gorman JM, Kent JM, Sullivan GM, Coplan JD (2000) Neuroanatomical hypothesis of panic disorder, revised. Am J Psychiatry 157(4):493–505
Gray J, Chabris C, Braver T (2003) Neural mechanisms of general fluid intelligence. Nat Neurosci 6:316–322
Kim JE, Dager SR, Lyoo IK (2012) The role of the amygdala in the pathophysiology of panic disorder: evidence from neuroimaging studies. Biol Mood Anxiety Disord 2:20
Lang PJ (1985) The cognitive psychophysiology of emotion: Anxiety and the anxiety disorders. Lawrence Erlbaum, New York
LeDoux JE (2000) Emotion circuits in the brain. Ann Rev Neurosci 23:155–184
Lueken U, Muehlhan M, Wittchen HU, Kellermann T, Reinhardt I, Konrad C, Lang T, Wittmann A, Ströhle A, Gerlach AL, Ewert A, Kircher T (2011) (Don’t) panic in the scanner! How panic patients with agoraphobia experience a functional magnetic resonance imaging session. Eur Neuropsychopharmacol 21:516–526
McCormick DA, Bal T (1994) Sensory gating mechanisms of the thalamus. Curr Opin Neurobiol 4:550–556
McNally RJ (2002) Anxiety sensitivity and panic disorder. Biol Psychiatry 52:938–946
Nagai M, Kishi K, Kato S (2007) Insular cortex and neuropsychiatric disorders: a review of recent literature. Eur Psychiatry 22:387–394
Oldfield RC (1971) The assessment and analysis of handedness: the Edingburgh inventory. Neuropsychologia 9:97–113
Paulus MP, Stein MB (2010) Interoception in anxiety and depression. Brain Struct Funct 214:451–463
Pennebaker J (1982) The psychology of physical symptoms. Springer, New York
Peterson RA, Reiss S (1992) Anxiety sensitivity index revised manual. In: Worthington OH (ed) Palos Heights, International Diagnostic Systems, Illinois
Pfleiderer B, Zinkirciran S, Arolt V, Heindel W, Deckert J, Domschke K (2007) fMRI amygdala activation during a spontaneous panic attack in a patient with panic disorder. World J Biol Psychiatry 8:269–272
Pfleiderer B, Zinkirciran S, Michael N, Hohoff C, Kersting A, Arolt V, Deckert J, Domschke K (2010) Altered auditory processing in patients with panic disorder—a pilot study. World J Biol Psychiatry 11:945–955
Pillay SS, Gruber SA, Rogowska J, Simpson N, Yurgelun-Todd DA (2006) fMRI of fearful facial affect recognition in panic disorder: the cingulate gyrus-amygdala connection. J Affect Disord 94:173–181
Pollatos O, Gramann K, Schandry R (2007a) Neural systems connecting interoceptive awareness and feelings. Hum Brain Mapp 28:9–18
Pollatos O, Herbert BM, Kaufmann C, Auer DP, Schandry R (2007b) Interoceptive awareness, anxiety and cardiovascular reactivity to isometric exercise. Int J Psychophysiol 65:167–173
Pollatos O, Schandry R, Auer DP, Kaufmann C (2007c) Brain structures mediating cardiovascular arousal and interoceptive awareness. Brain Res 1141:178–187
Richards JC, Bertram S (2000) Anxiety sensitivity, state and trait anxiety, and perception of change in sympathetic nervous system arousal. J Anxiety Disord 14:413–427
Sackeim HA, Greenberg MS, Weiman AL, Gur RC, Hungerbuhler JP, Geschwind N (1982) Hemispheric asymmetry in the expression of positive and negative emotions. Neurologic evidence. Arch Neurol 39:210–218
Schandry R (1981) Heartbeat perception and emotional experience. Psychophysiology 18:483–488
Schmidt NB, Santiago HT, Wernicke R (2001) Evaluating the etiology of anxiety sensitivity: relation to cardiovascular perception and reactivity. J Psychopathol Behav Assess 23:85–92
Schmidt NB, Zvolensky MJ, Maner JK (2006) Anxiety sensitivity: prospective prediction of panic attacks and axis I pathology. J Psychiatric Res 40:691–699
Schunck T, Erb G, Mathis A, Jacob N, Gilles C, Namer IJ, Meier D, Luthringer R (2008) Test-retest reliability of a functional MRI anticipatory anxiety paradigm in healthy volunteers. J Magn Reson Imaging 27:459–468
Shin LM, Liberzon I (2010) The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35:169–191
Slotnick SD, Moo LR, Segal JB, Hart J Jr (2003) Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Brain Res: Cog Brain Res 17:75–82
Somers J, Goldner E, Waraich P, Hsu L (2006) Prevalence and incidence studies of anxiety disorders: a systematic review of the literature. Can J Psychiatry 51:100–113
Stevens S, Gerlach A, Cludius B, Silkens A, Craske M, Hermann C (2011) Heartbeat perception in social anxiety before and during speech anticipation. Behav Res Ther 49:138–143
Stewart SH, Buffett-Jerrott SE, Kokaram R (2001) Heartbeat awareness and heart rate reactivity in anxiety sensitivity: a further investigation. J Anxiety Disord 15:535–553
Talairach J, Tournoux P (1988) Coplanar stereotactic atlas of the human brain. Thieme, New York
Tracy J, Goyal N, Flanders A, Weening R, Laskas J, Natale P, Waldron B (2007) Functional magnetic resonance imaging analysis of attention to one’s heartbeat. Psychosomat Med 69:952–960
Vanden Bogaerde A, De Raedt R (2008) Cognitive vulnerability in fear of flying: the role of anxiety sensitivity. Depress Anxiety 25:768–773
Vanden Bogaerde A, De Raedt R (2011) The moderational role of anxiety sensitivity in flight phobia. J Anxiety Disord 25:422–426
Waugh CE, Wager TD, Fredrickson BL, Noll DC, Taylor SF (2008) The neural correlates of trait resilience when anticipating and recovering from threat. Soc Cogn Affect Neurosci 3:322–332
Willem Van der Does AJ, Antony MM, Ehlers A, Barsky AJ (2000) Heartbeat perception in panic disorder: a reanalysis. Behav Res Ther 38:47–62
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This study was partially funded by the German Federal Ministry of Education and Research (BMBF; projects no. 01GV0611 (neuroimaging study) and No. 01GV0610) as part of the BMBF Psychotherapy Research Funding Initiative.
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Pfleiderer, B., Berse, T., Stroux, D. et al. Internal focus of attention in anxiety-sensitive females up-regulates amygdale activity: an fMRI study. J Neural Transm 121, 1417–1428 (2014). https://doi.org/10.1007/s00702-014-1248-5
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DOI: https://doi.org/10.1007/s00702-014-1248-5