Association between respiratory sinus arrhythmia and reductions in startle responding in three independent samples

Biological Psychology

Volumn 93, Issue 2, 2013, Pages 334-341

  Gorka, Stephanie M ^a   McGowan, Sarah Kate ^a   Campbell, Miranda L ^a   Nelson, Brady D ^a   Sarapas, Casey ^a   Bishop, Jeffrey R ^a   Shankman, Stewart A ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Habituation; Respiratory sinus arrhythmia; Startle

Indexed keywords

ADULT; AGE DISTRIBUTION; ANTICIPATION; ANXIETY; ARTICLE; ATTENTION; BLINKING; CARDIOPULMONARY FUNCTION; CONTROLLED STUDY; ETHNICITY; FEMALE; HABITUATION; HUMAN; HUMAN EXPERIMENT; MALE; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; RESPIRATORY SINUS ARRHYTHMIA; REST; SEX DIFFERENCE; STARTLE REFLEX; TASK PERFORMANCE;

ADOLESCENT; ANALYSIS OF VARIANCE; ANXIETY; ARRHYTHMIA, SINUS; ELECTROCARDIOGRAPHY; ELECTROENCEPHALOGRAPHY; ELECTROSHOCK; FEAR; FEMALE; HABITUATION, PSYCHOPHYSIOLOGIC; HUMANS; MALE; STARTLE REACTION; YOUNG ADULT;

EID: 84876738436     PISSN: 03010511     EISSN: 18736246     Source Type: Journal    
DOI: 10.1016/j.biopsycho.2013.03.003     Document Type: Article

References (78)

1. Aiken L.S., West S.G. Multiple Regression: Testing and Interpreting Interactions 1991, Sage, Newbury Park, CA.
2. Allen J.J.B., Chambers A.S., Towers D.N. The many metrices of cardiac chronotrophy: a pragmatic primer and a brief comparison of metrics. Biological Psychology 2007, 74:243-262. 10.1016/j.biopsycho.2006.08.005.
3. Allen M.T., Matthews K.A., Kenyon K.L. The relationships of resting baroreflex sensitivity, heart rate variability and measures of impulse control in children and adolescents. International Journal of Psychophysiology 2000, 37:185-194. 10.1016/S0167-8760(00)00089-1.
4. Baas J.M.P., Grillon C., Böcker K.B.E., Brack A.A., Morgan C.A., Kenemans J.L., Verbaten M.N. Benzodiazepines have no effect on fear-potentiated startle in humans. Psychopharmacology 2002, 161:233-247. 10.1007/s00213-002-1011-8.
5. Bar-Haim Y., Lamy D., Pergamin L., Bakermans-Kranenburg M.J., van Ijzendoorn M.H. Threat-related attentional bias in anxious and non-anxious individuals: a meta-analytic study. Psychological Bulletin 2007, 133:1-24. 10.1037/0033-2909.133.1.1.
6. Barlow D.H. Anxiety and Its Disorders: The Nature and Treatment of Anxiety and Panic 2002, The Guilford Press, New York.
7. Berntson G.G., Sarter M., Cacioppo J.T. Anxiety and cardiovascular reactivity: the basal forebrain cholinergic link. Behavioural Brain Research 1998, 94:225-248. 10.1016/S0166-4328(98)00041-2.
8. Beauchaine T. Vagal tone, development, and Gray's motivational theory: toward an integrated model of autonomic nervous system functioning in psychopathology. Developmental Psychopathology 2001, 13:183-214. 10.1017/S0954579401002012.
9. Bertsch K., Hagemann D., Naumann E., Schachinger H., Schulz A. Stability of heart rate variability indices reflecting parasympathetic activity. Psychophysiology 2012, 49:672-682. 10.1111/j.1469-8986.2011.01341.x.
10. Blom E.H., Olsson E.M., Serlachius E., Ericson M., Ingvar M. Heart rate variability (HRV) in adolescent females with anxiety disorders and major depressive disorder. Acta Paediatrica 2010, 99:604-611. 10.1111/j.1651-2227.2009.01657.x.
11. Blumenthal T.D. The startle response to acoustic stimuli near startle threshold: effects of stimulus rise and fall time, duration, and intensity. Psychophysiology 1988, 25:607-611. 10.1111/j.1469-8986.1988.tb01897.x.
12. Blumenthal T.D. Inhibition of the human startle response is affected by both prepulse intensity and eliciting stimulus intensity. Biological Psychology 1996, 44:85-104. 10.1016/0301-0511(96)05214-3.
13. Blumenthal T.D., Cuthbert B.N., Filion D.L., Hackley S., Lipp O.V., van Boxtel A. Committee report: guidelines for human startle eyeblink electromyographic studies. Psychophysiology 2005, 42:1-15. 10.1111/j.1469-8986.2005.00271.x.
14. Bradley M.M., Cuthbert B.N., Lang P.J. Affect and the startle reflex. Startle Modification: Implication for Neuroscience, Cognitive Science, and Clinical Science 1999, Cambridge University Press, New York. M.E. Dawson, A.M. Schell, A.H. Bohmet (Eds.).
15. Casadei B., Moon J., Johnston J., Caiazza A., Sleight P. Is respiratory sinus arrhythmia a good index of cardiac vagal tone in exercise?. Journal of Applied Physiology 1996, 81:556-564.
16. Cohen H., Kotler M., Matar M.A., Kaplan Z., Loewenthal U., Miodownik H., Cassuto Y. Analysis of heart rate variability in posttraumatic stress disorder patients in response to a trauma related reminder. Biological Psychiatry 1998, 44:1054-1059. 10.1016/S0006-3223(97)00475-7.
17. Craske M.G., Kircanski K., Zelikowski M., Mystkowski J., Chowdhury N., Baker A. Optimizing inhibitory learning during exposure therapy. Behaviour Research and Therapy 2008, 46:5-27. 10.1016/j.brat.2007.10.003.
18. Creamer M., Burgess P., Pattison P. Reaction to trauma: a cognitive processing model, Journal of. Abnormal Psychology 1992, 101:452-459. 10.1037/0021-843X.101.3.452.
19. Deacon B.J., Abramowitz J.S. Cognitive and behavioral treatments for anxiety disorders: a review of meta-analytic findings. Journal of Clinical Psychology 2004, 60:429-441. 10.1002/jclp.10255.
20. Demaree H.A., Robinson D.L., Everhart D.E., Schmeichel B.J. Resting RSA is associated with natural and self-regulated responses to negative emotional stimuli. Brain and Cognition 2004, 56:14-23. 10.1016/j.bandc.2004.05.001.
21. Denver J.W., Reed S.F., Porges S.W. Methodological issues in the quantification of respiratory sinus arrhythmia. Biological Psychology 2007, 74:286-294. 10.1016/j.biopsycho.2005.09.00.
22. Eckman P.S., Shean G.D. Habituation of cognitive and physiological arousal and social anxiety. Behavior Research and Therapy 1997, 35:1113-1121. 10.1016/S0005-7967(97)80005-8.
23. Ellwanger J., Geyer M.A., Braff D.L. The relationship of age to prepulse inhibition and habituation of the acoustic startle response. Biological Psychology 2003, 62:175-195. 10.1016/S0301-0511(02)00126-6.
24. Fabes R.A., Eisenberg N. Regulatory control and adults' stress-related responses to daily life events. Journal of Personality and Social Psychology 1997, 73:1107-1117. 10.1037/0022-3514.73.5.1107.
25. Feingold A. Gender differences in personality: a meta-analysis. Psychological Bulletin 1994, 116:429-456. 10.1037/0033-2909.116.3.429.
26. Foa E.B., Kozak M.J. Emotional processing of fear: exposure to corrective information. Psychological Bulletin 1986, 99:20-35. 10.1037/0033-2909.99.1.20.
27. Frazier T.W., Strauss M.E., Steinhauer S.R. Respiratory sinus arrhythmia as an indicator of emotional response in young adults. Psychophysiology 2004, 41:75-83. 10.1046/j.1469-8986.2003.00131.x.
28. Friedman B.H. An autonomic flexibility-neurovisceral integration model of anxiety and cardiac vagal tone. Biological Psychology 2007, 74:185-199. 10.1016/j.bbr.2011.03.031.
29. Grillon C., Ameli R. Effects of threat of shock, shock electrode placement and darkness on startle. International Journal of Psychophysiology 1998, 28:223-231. 10.1016/S0167-8760(97)00072-X.
30. Grillon C., Baas J.M.P., Pine D.S., Lissek S., Lawley M., Ellis V., Levine J. The benzodiazepine alprazolam dissociates contextual fear from cued fear in humans as assessed by fear-potentiated startle. Biological Psychiatry 2006, 60:760-766. 10.1016/j.biopsych.2005.11.02.
31. Gross J.J. Emotion regulation: past, present, future. Cognition and Emotion 1999, 13:551-573. 10.1080/026999399379186.
32. Grossman P., Karemaker J., Wieling W. Prediction of tonic parasympathetic cardiac control using respiratory sinus arrhythmia: the need for respiratory control. Psychophysiology 1990, 28:201-216. 10.1111/j.1469-8986.1991.tb00412.x.
33. Grossman P., Kollai M. Respiratory sinus arrythymia, cardiac vagal tone, and respiration: within- and between-individual relations. Psychophysiology 1993, 30:486-495. 10.1111/j.1469-8986.1993.tb02072.x.
34. Grossman P., Taylor E.W. Toward understanding respiratory sinus arrhythmia: relations to cardiac vagal tone, evolution and biobehavioral functions. Biological Psychology 2007, 74:263-285. 10.1016/j.biopsycho.2005.11.014.
35. Groves P.M., Thompson R.F. Habituation: a dual-process theory. Psychological Review 1970, 77:419-450. 10.1037/h0029810.
36. Hatfield B.D., Santa Maria D.L., Porges S.W., Potts J.T., Spalding T., Byrne E.A. Respiratory sinus arrhythmia during exercise in aerobically trained and untrained men. Medicine & Science in Sports & Exercise 1998, 30:206-214. 10.1097/00005768-199802000-00006.
37. Herry C., Ferraguti F., Singewald N., Letzkus J.J., Ehrlich I., Lüthi A. Neuronal circuits of fear extinction. European Journal of Neuroscience 2010, 31:599-612. 10.1111/j.1460-9568.2010.07101.x.
38. Hoenig K., Hochrein A., Quednow B.B., Maier W., Wagner M. Impaired prepulse inhibition of acoustic startle in obsessive compulsive disorder. Biological Psychology 2005, 10:1153-1158. 10.1016/j.biopsych.2005.01.040.
39. Hofmann S.G., Moscovitch D.A., Litz B.T., Kim H., Davis L.L., Pizzagalli D.A. The worried mind: autonomic and prefrontal activation during worrying. Emotion 2005, 5:464-475. 10.1037/1528-3542.5.4.464.
40. Houtveen J.H., Rietveld S., De Geus E.J.C. Contribution of tonic vagal modulation of heart rate, central respiratory drive, respiration depth, and respiratory frequency to respiratory sinus arrhythmia during mental stress and physical exercise. Psychophysiology 2002, 39:427-436. 10.1017/S0048577202394022.
41. Johnsen B.H., Hansen A.L., Sollers J.J., Murison R., Thayer J.F. Heart rate variability is inversely related to cortisol reactivity during cognitive stress. Psychosomatic Medicine 2002, 64:289.
42. Jovanovic T., Norrholm S.D., Sakoman A.J., Esterajher S., Kozarić-Kovačić D. Altered resting psychophysiology and startle response in Croatian combat veterans with PTSD. International Journal of Psychophysiology 2009, 71:264-268. 10.1016/j.ijpsycho.2008.10.007.
43. Klein D.N., Leon A.C., Li C., D'Zurilla T.J., Black S.R., Vivian D., Dowling F., Arnow B.A., Manber R., Markowitz J.C., Kocsis J.H. Social problem solving and depressive symptoms over time: a randomized clinical trial of cognitive-behavioral analysis system of psychotherapy, brief supportive psychotherapy, and pharmacotherapy. Journal of Consulting and Clinical Psychology 2011, 79:342-352. 10.1037/a0023208.
44. Lang P.J. The emotion probe: studies of motivation and attention. American Psychologist 1995, 50:372-385. 10.1037/0003-066X.50.5.372.
45. LaRowe S.D., Patrick C.J., Curtin J.J., Kline J.P. Personality correlates of startle habituation. Biological Psychology 2006, 72:257-264. 10.1016/j.biopsycho.2005.11.008.
46. LeDoux J. The Emotional Brain 1996, Touchstone Simon and Schuster, New York, NY.
47. Licht C.M.M., de Geus J.C.N., van Dyck R., Penninx B.W.J.H. Association between anxiety disorders and heart rate variability in the Netherlands Study of Depression and Anxiety (NESDA). Psychosomatic Medicine 2009, 71:508-518. 10.1097/PSY.0b013e3181a292a6.
48. Ludewig S., Ludewig K., Geyer M.A., Hell D., Vollenweider F.X. Prepulse inhibition deficits in patients with panic disorder. Depression and Anxiety 2002, 15:55-60. 10.1002/da.10026.
49. Melzig C.A., Weike A.I., Hamm A.O., Thayer J.F. Individual differences in fear-potentiated startle as a function of resting heart rate variability: implications for panic disorder. International Journal of Psychophysiology 2009, 71:109-117. 10.1016/j.ijpsycho.2008.07.013.
50. Murata T., Takahashi T., Hamada T., Omori M., Kosaka H., Yoshida H., Wada Y. Individual trait anxiety levels characterizing the properties of Zen meditation. Neuropsychobiology 2004, 50:189-194. 10.1159/000079113.
51. Myers K.M., Davis M. Mechanisms of fear extinction. Molecular Psychiatry 2007, 12:120-150. 10.1111/1467-8721.00166.
52. Nelson B.D., Shankman S.A. Does intolerance of uncertainty predict anticipatory startle responses to uncertain threat?. International Journal of Psychophysiology 2011, 81:107-115. 10.1016/j.ijpsycho.2011.05.003.
53. Oken B.S., Salinsky M.C., Elsas S.M. Vigilance, alertness, or sustained attention: physiological basis and measurement. Clinical Neurophysiology 2006, 117:1885-1901. 10.1016/j.clinph.2006.01.017.
54. Pacheco-Unguetti A.P., Acosta A., Callejas A., Lupiáñez J. Attention and anxiety different attentional functioning under state and trait anxiety. Psychological Science 2010, 21(2):298-304. 10.1177/0956797609359624.
55. Porges S.W. Orienting in a defensive world: mammalian modifications of our evolutionary heritage, a polyvagal theory. Psychophysiology 1995, 32:301-318.
56. Porges S.W. Emotion: an evolutionary by-product of the neural regulation of the autonomic nervous system. Annals of New York Academy of Sciences 1997, 807:62-77. 10.1111/j.1749-6632.1997.tb51913.x.
57. Porges S.W. The polyvagal theory: phylogenetic substrates of a social nervous system. International Journal of Psychophysiology 2001, 42:123-146. 10.1016/S0167-8760(01)00162-3.
58. Porges S.W. The polyvagal perspective. Biological Psychology 2007, 74:116-143. 10.1016/j.biopsycho.2006.06.009.
59. Porges S.W., Bohrer R.E. Analyses of periodic processes in psychophysiological research. Principles of Psychophysiology: Physical, Social, and Inferential Elements 1990, 708-753. Cambridge University Press, New York. J.T. Cacioppo, L.G. Tassinary (Eds.).
60. Porges S.W., Doussard-Roosevelt J.A., Maiti A.K. Vagal tone and the physiological regulation of emotion. Monographs of the Society for Research in Child Development 1994, 167-186. Blackwell Publishing, Boston. N.A. Fox (Ed.).
61. Porges S.W., Raskin D.C. Respiratory and heart rate components of attention. Journal of Experimental Psychology 1969, 81:497-503. 10.1037/h0027921.
62. Rankin C., Abrams T., Barry R., Bhatnagar S., Clayton D., Colombo J., Coppola G., Geyer M.A., Glanzman D.L., Marsland S., McSweeney F.K., Wilson D.A., Wu C.F., Thompson R. Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiology of Learning and Memory 2009, 92(2):135-138. 10.1016/j.nlm.2008.09.012.
63. Raskin M. Decreased skin conductance response habituation in chronically anxious patients. Biological Psychology 1975, 2:309-319. 10.1016/03010511(75)90039-3.
64. Ross R.J., Ball W.A., Cohen M.E., Silver S.M., Morrison A.R., Dinges D.F. Habituation of the startle reflex in post-traumatic stress disorder. Journal of Neuropsychiatry and Clinical Neurosciences 1989, 1:305-307.
65. Roth W.T., Ehlers A., Taylor C.B., Margraf J., Agras W.S. Skin conductance habituation in panic disorder patients. Biological Psychiatry 1990, 27:1231-1243. 10.1016/0006-3223(90)90421-W.
66. Rothbaum B.O., Kozak M.J., Foa E.B., Whitaker D.J. Posttraumatic stress disorder in rape victims: autonomic habituation to auditory stimuli. Journal of Traumatic Stress 2001, 14:283-293. 10.1023/A:1011160800958.
67. Ruiz-Padial E., Sollers J.J., Vila J., Thayer J.F. The rhythm of the heart in the blink of an eye: emotion-modulated startle magnitude covaries with heart rate variability. Psychophysiology 2003, 40:306-313. 10.1111/1469-8986.00032.
68. Sarapas, C., Shankman, S.A., Nelson, B.D., Campbell, M.L., Bishop, J.R., Robison-Andrew, J., Altman, S.E., Gorka, S.M., Katz, A.C. Are appetitive and defensive motivation related? A psychophysiological examination in two independent samples, under review.
69. Sargunaraj D., Lehrer P.M., Hochron S.M., Rausch L., Edelberg R., Porges S.W. Cardiac rhythm effects of .125-Hz paced breathing through a resistive load: implications for paced breathing therapy and the polyvagal theory. Applied Psychophysiology, and Biofeedback 1996, 21:131-147. 10.1007/BF02284692.
70. Scherbaum C.A., Ferreter J.M. Estimating statistical power and required sample sizes for organizational research using multilevel modeling. Organization Research Methods 2009, 12:347-367. 10.1177/1094428107308906.
71. Segerstrom S.C., Nes L.S. Heart rate variability reflects self-regulatory strength, effort, and fatigue. Psychological Science 2007, 18:275-281. 10.1111/j.1467-9280.2007.01888.x.
72. Siddle D.A. Orienting, habituation, and resource allocation: an associative analysis. Psychophysiology 1991, 28:245-259. 10.1111/j.1469-8986.1991.tb02190.x.
73. Thayer J.F., Friedman B.H., Borkovec T.D. Autonomic characteristics of generalized anxiety disorder and worry. Biological Psychiatry 1996, 39:255-266. 10.1016/0006-3223(95)00136-0.
74. Thayer J.F., Lane R.D. A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders 2000, 61:201-216. 10.1016/S0165-0327(00)00338-4.
75. Thayer J.F., Lane R.D. Claude Bernard and the heart-brain connection: further elaboration of a model of neurovisceral integration. Neuroscience & Biobehavioral Reviews 2009, 33:81-88. 10.1016/j.neubiorev.2008.08.004.
76. Weinstein S.E., Quigley K.S. Locus of control predicts appraisals and cardiovascular reactivity to a novel active coping task. Journal of Personality 2006, 74:911-931. 10.1111/j.1467-6494.2006.00396.x.
77. Werner K.W., Gross J.J. Emotion regulation and psychopathology: a conceptual framework. Emotion Regulation and Psychopathology 2009, The Guilford Press, New York. A. Kring, D. Sloan (Eds.).
78. Yeragani V.K., Pohl R., Berger R., Balon R., Ramesh C., Glitz D., Srinivasan K., Weinberg P. Decreased heart rate variability in panic disorder patients: a study of power-spectral analysis of heart rate. Psychiatry Research 1993, 46:89-103. 10.1016/0165-1781(93)90011-5.