Prefrontal-limbic connectivity during worry in older adults with generalized anxiety disorder

Aging and Mental Health

Volumn 21, Issue 4, 2017, Pages 426-438

  Mohlman, Jan ^a   Eldreth, Dana A ^b   Price, Rebecca B ^c   Staples, Alison M ^d   Hanson, Catherine ^b  

^a WILLIAM PATERSON UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

aging; GAD; generalized anxiety disorder; neurobiology; prefrontal limbic connectivity; worry

Indexed keywords

AGED; ANXIETY; ANXIETY DISORDER; BRAIN MAPPING; FEMALE; HUMAN; LIMBIC CORTEX; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PROCEDURES; PSYCHOLOGY;

AGED; ANXIETY; ANXIETY DISORDERS; BRAIN MAPPING; FEMALE; HUMANS; LIMBIC LOBE; MAGNETIC RESONANCE IMAGING; MALE; PREFRONTAL CORTEX;

EID: 84946866377     PISSN: 13607863     EISSN: 13646915     Source Type: Journal    
DOI: 10.1080/13607863.2015.1109058     Document Type: Article

References (82)

1. Andor, T., Gerlach, A.L., & 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. Journal of Abnormal Psychology, 117, 193–205.
2. Andreescu, C., Butters, M., Lenze, E.J., Venkatraman, V.K., Nable, M., Reynolds, C.F. III, & Aizenstein, H.J., (2009). FMRI activation in anxious depression:A potential biomarker. International Journal of Geriatric Psychiatry, 24, 820–828.
3. Andreescu, C., Gross, J.J., Lenze, E.J., Edelman, K.D., Snyder, S., Tanase, C., Aizenstein, H. (2011a). Altered cerebral blood flow patterns associated with pathologic worry in the elderly. Depression & Anxiety, 28, 202–209.
4. Andreescu, C., Sheu, L.K., Tudorascu, D., Gross, J.J., Walker, S., Banibasbemi, L., & Aizenstein, H., (2015). Emotion reactivity and regulation in late-life generalized anxiety disorder:Functional connectivity at baseline and post-treatment. American Journal of Geriatric Psychiatry, 23, 200–214.
5. Andreescu, C., Wu, M., Butters, M.A., Figurski, J., & Reynolds, C.F., (2011b). The default mode network in late life anxious depression. American Journal of Geriatric Psychiatry, 19, 980–983.
6. Ayers, C.R., Sorrell, J.T., Thorp, S.R., & Wetherell, J.L., (2007). Evidence-based psychological treatments for late life anxiety. Psychology and Aging, 22, 8–17.
7. Ballenger, J.C., Davidson, J.R.T., Lecrubier, Y., Nutt, D.J., Borkovec, T.D., Rickels, K., … Wittchen, H.-U., (2001). Consensus statement on generalized anxiety disorder from the International Consensus Group on Depression and Anxiety. Journal of Clinical Psychiatry, 62(suppl. 11), 53–58.
8. Basevitz, P., Pushkar, D., Chaikelson, J., Conway, M., & Dalton, C., (2008). Age-related differences in worry and related processes. International Journal of Aging & Human Development, 66, 283–305.
9. Beck, A.T., & Steer, R.A., (1987). Manual for the revised beck depression inventory. San Antonio, TX:Psychological Corporation.
10. Beck, A.T., & Steer, R.A., (1990). Manual for the beck anxiety inventory. San Antonio, TX:Psychological Corporation.
11. Beckmann, C.F., Jenkinson, M., & Smith, S.M., (2003). General multi-level linear modeling for group analysis in FMRI. NeuroImage, 20, 1052–1063.
12. Beekman, A.T.F., Bremmer, M.A., Deeg, D.J.H., van Balkom, A.J.L.M., Snut, J.H., deBeurs, E., … van Tilburg, W., (1998). Anxiety disorders in later life:A report from the Longitudinal Aging Study Amsterdam. International Journal of Geriatric Psychiatry, 13, 717–726.
13. Behar, E., DiMarco, I., Hekler, E., Mohlman, J., & Staples, A., (2009). Current theoretical models of generalized anxiety disorder (GAD):Conceptual review and treatment implications. Journal of Anxiety Disorders, 23, 1011–1023.
14. Borkovec, T.D., (1994). The nature, functions, and origins of worry. In G., Davey & F., Tallis (Eds.), Worrying:Perspectives on theory, assessment, and treatment (pp. 5–33). Sussex:Wiley & Sons.
15. Borkovec, T.D., & Inz, J., (1990). The nature of worry in generalized anxiety disorder:A predominance of thought activity. Behaviour Research and Therapy, 28, 153–158.
16. Brenes, G.A., Guralnik, J.M., Williamson, J., Fried, L.P., & Penninx, B.W.J.H., (2005). Correlates of anxiety symptoms in physically disabled older women. American Journal of Geriatric Psychiatry, 13, 15–22.
17. Campbell-Sills, L., Simmons, A.N., Lovero, K.L., Rochlin, A.A., Paulus, M.P. & Stein, M.B. (2011). Functioning of neural systems supporting emotion regulation in anxiety-prone individuals. NeuroReport, 54, 689–696
18. Cribben, I., Haraldsdottir, R., Atlas, L.Y., Wager, T.D., & Lindquist, M.A., (2012). Dynamic connectivity regression:Determining state-related changes in brain connectivity. Neuroimage, 61, 907–920.
19. Delgado, M.R., Nearing, K.I., LeDoux, J.E., & Phelps, E.A., (2008). Neural circuitry underlying the regulation of conditioned fear and its relation to extinction. Neuron, 59, 829–838.
20. DiNardo, P., Brown, T.A., & Barlow, D.H., (1994). Anxiety Disorders Interview Schedule for DSM IV–Revised (ADIS-IV-R). Albany, NY. Phobia and Anxiety Disorders Clinic, State University of New York.
21. Drevets, W.C., Price, J.L., Simpson, J.R., Todd, R.D., Vannier, M., & Raichle, M.E., (1997). Subgenual prefrontal cortex abnormalities in mood disorders. Nature, 386, 824–827. 215–226.
22. Engels, A.S., Heller, W., Mohanty, A., Herrington, J.D., Banich, M.T., Webb, A.G., Miller, G.A., (2007). Specificity of regional brain activity in anxiety types during emotion processing. Psychophysiology, 44, 352–363.
23. Etkin, A., Prater, K.E., Schatzberg, A.F., Menon, V., & Greicius, M.D., (2009). Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Archives of General Psychiatry, 66, 1361–1372.
24. Etkin, A., & Wager, T.D., (2007). Functional neuroimaging of anxiety:A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry, 164, 1476–1488.
25. First, M.B., Gibbon, M., Spitzer, R.L., & Williams, J.B.W. (1995). Structured clinical interview for DSM-IV Axis I disorders (SCID-I, version 2.0, Final Version). New York, NY:Biometrics Department, New York State Psychiatric Institute.
26. First, M.B., Gibbon, M., Spitzer, R.L., & Williams, J.B.W., (2001). Structured clinical interview for DSM-IV-TR Axis I disorders (SCID-I, Final Version). New York, NY:Biometrics Department, New York State Psychiatric Institute.
27. Flint, A., (1994). Epidemiology and comorbidity of anxiety disorders in the elderly. American Journal of Psychiatry, 151, 640–649.
28. Flint, A., (1999). Anxiety disorders in late life. Canadian Family Physician, 45, 2672–2679.
29. Flint, A.J., (2005). Generalised anxiety disorder in elderly patients:Epidemiology, diagnosis and treatment options. Drugs and Aging, 22, 101–114.
30. Folstein, S.E., Folstein, M.F., & McHugh, P.R., (1975). ‘Mini-mental state’:A practical method for grading the mental state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.
31. Glymour, C., Scheines, R., Spirtes, P., & Ramsey, J., (2010). Tetrad IV. http://www.phil.cmu.edu/projects/tetrad/tetrad4.html.
32. Goldin, P.R., McRae, K., Ramel, W., & Gross, J.J., (2008). The neural bases of emotion regulation:Reappraisal and suppression of negative emotion. Biological Psychiatry, 63, 577–586.
33. Hasher, L., Stolzfus, E.R., Zacks, R.T., & Rypma, B., (1991). Age and inhibition. Journal of Experimental Psychology:Learning, Memory, and Cognition, 17, 163–169.
34. Hasher, L., & Zacks, R.T., (1988). Working Memory, comprehension, and aging:A review and new view. In G.H., Bower (Ed.), The Psychology of learning and motivation (Vol. 22, pp. 193–225). San Diego, CA:Academic Press.
35. Hamann, S., & Mao, H., (2002). Positive and negative emotional verbal stimuli elicit activity in the left amygdala. Brain Imaging, 13, 15–19.
36. Hasson, U., Nir, Y., Levy, I., Fuhrmann, G., & Malach, R., (2004). Intersubject synchronization of cortical activity during natural vision. Science, 303, 1634–1640.
37. Hayes, S., Hirsch, C., & Mathews, A., (2008). Restriction of working memory capacity during worry. Journal of Abnormal Psychology, 117, 712–717.
38. Hoehn-Saric, R., Lee, J.S., McLeod, D.R., & Wong, D.F., (2005). Effect of worry on regional cerebral blood flow in nonanxious subjects. Psychiatry Research:Neuroimaging, 140, 259–269.
39. Hoehn-Saric, R., Schlund, M.W., & Wong, S.H.Y., (2004). Effects of citalopram on worry and brain activation in patients with generalized anxiety disorder. Psychiatry Research:Neuroimaging, 131, 11–21.
40. Hoyer, J., Becker, E.S., & Roth, W.T., (2000). Characteristics of worry in GAD patients, social phobics, and controls. Depression & Anxiety, 13, 89–96.
41. Hu, S., Chao, H.A., Zhang, S., Ide, J.S., & Li, C.-S.R. (2014). Changes in cerebral morphometry and amplitude of low-frequency fluctuations of BOLD signals during healthy aging:Correlation with inhibitory control. Brain Structure & Function, 219, 983–994.
42. Koenigsberg, H.W., Fan, J., Ochsner, K.N., Liu, X., Guise, K.G., Pizzarello, S., … Siever, L.J., (2009). Neural correlates of the use of psychological distancing to regulate responses to negative social cues. Neuropsychologia, 48, 854–863.
43. Kumar, A., Haroon, E., Darwin, C., Pham, D., Ajilore, O., Rodriguez, G., & Mintz, J., (2008). Gray matter prefrontal changes in type 2 diabetes detected using MRI. Journal of Magnetic Resonance Imaging, 27, 14–19.
44. LeDoux, J.E., (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184.
45. Lenze, E.J., Mulsant, B.H., Mohlman, J., Shear, K., Dew, M.A., Schulz, R., … Reynolds, C.F. III., (2005). Generalized anxiety disorder in late life:Longitudinal course and comorbidity with major depressive disorder. American Journal of Geriatric Psychiatry, 13, 77–80.
46. Martens, E.J., deJong, P., Na, B., Cohen, B.E., Lett, H., & Whooley, M.A., (2010). Generalized anxiety disorder and cardiovascular events in patients with stable coronary heart disease:The Heart and Soul Study. Archives of General Psychiatry, 67, 750–758.
47. Meek, C. (1996). Selecting graphical models:Causal and statistical modeling (Unpublished dissertation). Carnegie-Mellon University, Pittsburgh, PA.
48. Meyer, T., Miller, M., Metzger, R., & Borkovec, T.D., (1990). Development and validity of the Penn State Worry Scale. Behaviour Research & Therapy, 28, 487–495.
49. Miller, E., (1984). Verbal fluency as a function of a measure of verbal intelligence in relation to different types of pathology. British Journal of Clinical Psychology, 23, 53–57.
50. Mitte, K., Noack, P., Stell, R., & Hautzinger, M., (2005). A meta-analytic review of the efficacy of drug treatment in generalized anxiety disorder. Journal of Clinical Psychopharmacology, 25, 141–150.
51. Mohlman, J., (2004). Psychosocial treatment of late life generalized anxiety disorder:Current status and future directions. Clinical Psychology Review, 24, 149–169.
52. Mohlman, J., Price, R., Eldreth, D.A., Chazin, D., Glover, D., & Kates, W.R., (2009). The relation of worry to prefrontal cortex volume in late life generalized anxiety disorder. Psychiatry Research:Neuroimaging, 173, 121–127.
53. Nee, D.E., Wager, T.D., & Jonides, J., (2007). Interference resolution:Insights from a meta-analysis of neuroimaging tasks. Cognitive, Affective, and Behavioral Neuroscience, 7, 1–17.
54. Newman, M.G., Zuellig, A.R., Kachin, K.E., Constantino, M.J., Przeworski, A., Ericson, T., & Cashman-McGrath, L., (2002). Preliminary reliability and validity of the Generalized Anxiety Disorder Questionnaire-IV:A revised self-report diagnostic measure of generalized anxiety disorder. Behavior Therapy, 33, 215–233.
55. Nitschke, J.B., Heller, W., & Miller, G.A., (2000). Anxiety, stress, and cortical brain function. In J.C., Borod (Ed.), The neuropsychology of emotion (pp. 298–319). New York, NY:Oxford University Press.
56. Ochsner, K.N., Bunge, S.A., Gross, J.L., & Gabrieli, J.D.E., (2002). Rethinking feelings:An fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience, 14, 1215–1229.
57. Ochsner, K.N., & Gross, J.J., (2008). Cognitive emotion regulation:Insights from social cognitive and affective neuroscience. Current Directions in Psychological Science, 17, 153–158.
58. Parè, D., Royer, S., Smith, Y., & Lang, E.J., (2003). Contextual inhibitory gating of impulse traffic in the intra-amygdaloid network. Annals of the New York Academy of Science, 985, 78–91.
59. Paulesu, E., Sambugaro, E., Torti, T., Danelli, L., Ferri, F., Scialfa, G., … Sassaroli, S., (2010). Neural correlates of worry in generalized anxiety disorder and in normal controls:A functional MRI study. Psychological Medicine, 40, 117–124.
60. Phelps, E.A., O'Connor, K.J., Gatenby, C., Gore, J.C., Grillon, C., & Davis, M., (2001). Activation of the left amygdala to a cognitive representation of fear. Nature Neuroscienc, 4, 437–441.
61. Raz, N., Gunning-Dixon, F., Head, D., Rodrigue, K.M., Williamson, A., & Acker, J.D., (2004). Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex:Replicability of regional differences in volume. Neurobiology of Aging, 25, 377–396.
62. Ramsey, J.D., Hanson, S.J., Hanson, C., Halchenko, Y.O., Poldrack, R.A., & Glymour, C., (2010). Six problems for causal inference from fMRI. NeuroImage, 49(2), 1545–1558.
63. Reuter-Lorenz, P.A., & Mikels, J.A., (2006). The aging mind and brain:Implications of enduring plasticity for behavioral and cultural change. In P.B., Baltes, P., Lorenz, & F., Rosier (Eds.), Lifespan development and the brain (pp. 255–276). Cambridge:Cambridge University Press.
64. Ross, T.P., Lichtenberg, P.A., & Christensen, B.K., (1995). Normative data on the Boston Naming Test for elderly adults in a demographically diverse medical sample. Clinical Neuropsychologist, 9, 321–325.
65. Salerno, J.A., Murphy, D.G., Horwitz, B., DeCarli, C., Haxby, J.V., & Rapoport, S.I., (1992). Brain atrophy in hypertension:A volumetric magnetic resonance imaging study. Hypertension, 20, 340–348.
66. Schwarz, G., (1978). Estimating the dimension of a model. Annals of Statistics, 6, 451–464.
67. Servaas, M.N., Riese, H., Ormel, J., & Aleman, A. (2014). The neural correlates of worry in association with individual differences in neuroticism. Human Brain Mapping, 35, 4303–4315.
68. Skarborn, M., & Nicki, R., (2000). Worry in pre- and post-retirement persons. International Journal of Aging & Human Development, 50, 61–71.
69. Trenerry, M.R., Crosson, B., DeBoe, J., & Leber, W.R., (1989). Stroop neuropsychological screening test manual. Odessa, FL:Psychological Assessment Resources.
70. Urry, H.L., van Reekum, C.M., Johnstone, T., Kalin, N.H., Thurow, M.E., Schaefer, H.S., … Davidson, R.J., (2006). Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. Journal of Neuroscience, 26, 4415–4425.
71. Van Hout, H.P.J., Beekman, A.T.F., DeBeurs, E., Comijs, H., Van Marwijk, H., DeHaan, M., & Deeg, D.J.H., (2004). Anxiety and the risk of death in older men and women. British Journal of Psychiatry, 185, 399–404.
72. Wager, T.D., Jonides, J., Smith, E.E., & Nichols, T.E., (2005). Toward a taxonomy of attention shifting:Individual differences in fMRI during multiple shift types. Cognitive Affective and Behavioral Neuroscience, 5, 127–143.
73. Wager, T.D., Waugh, C.E., Lindquist, M., Noll, D.C., Fredrickson, B.L., & Taylor, S.F., (2009a). Brain mediators of cardiovascular responses to social threat, Part II:prefrontal subcortical pathways and relationship with anxiety. Neuroimage, 47, 836–851.
74. Wager, T.D., Waugh, C.E., Lindquist, M., Noll, D.C., Fredrickson, B.L., & Taylor, S.F., (2009b). Brain mediators of cardiovascular responses to social threat, Part I:Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate variability. Neuroimage, 47, 821–835.
75. Wagner, A.D., Maril, A., Bjork, R.A., & Schacter, D.L., (2001). Prefrontal contributions to executive control:fMRI evidence for functional distinctions within lateral Prefrontal cortex. Neuroimage, 14, 1337–1347.
76. Wechsler, D., (1997). Wechsler adult intelligence scale and wechsler memory scale technical manual (3rd ed.). San Antonio, TX:The Psychological Corporation.
77. Wendt, J., Lotze, M., Weike, A.I., Hosten, N., & Hamm, A.O., (2008). Brain activation and defensive response mobilization during sustained exposure to phobia-related and other affective pictures in spider phobia. Psychophysiology, 45, 205–215.
78. West, R.L., (1996). An application of prefrontal cortex function theory to cognitive aging. Psychological Bulletin, 120, 272–292.
79. Woolrich, M.W., Behrens, T.E.J., Beckmann, C.F., Jenkinson, M., & Smith, S.M., (2004). Multi-level linear modelling for FMRI group analysis using Bayesian inference. NeuroImage, 21, 1732–1747.
80. Worsley, K.J., (2001). Statistical analysis of activation images. In P., Jezzard, P.M., Matthews and S.M., Smith (Eds.), Functional MRI:An introduction to methods. Oxford:Oxford University Press. chapter 14.
81. Zayfert, C., Dums, A.R., Ferguson, R.J., & Hegel, M.T., (2002). Health functioning impairments associated with posttraumatic stress disorder, anxiety disorders, and depression. Journal of Nervous & Mental Disease, 190, 233–240.
82. Zinbarg, R.E., Craske, M.G., & Barlow, D.H., (2006). Mastery of your anxiety and worry:Therapists' guide. New York, NY:Oxford University Press.