Circuit-wide structural and functional measures predict ventromedial prefrontal cortex fear generalization: Implications for generalized anxiety disorder

Journal of Neuroscience

Volumn 34, Issue 11, 2014, Pages 4043-4053

  Cha, Jiook ^a,e   Greenberg, Tsafrir ^a   Carlson, Joshua M ^b,c   DeDora, Daniel J ^b   Hajcak, Greg ^a   Mujica Parodi, Lilianne R ^a,b,d  

^a STONY BROOK UNIVERSITY   (United States)

^b St Francis Hospital The Heart Center   (United States)

^c NORTHERN MICHIGAN UNIVERSITY   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e Department of Psychiatry Columbia University College of Physicians and Surgeons The New York State Psychiatry Institute ^*  (United States)

Author keywords

Anxiety; Connectivity; Fear conditioning; Fear generalizaton; Resting state; Tractography

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; BRAIN STRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CORTICAL THICKNESS (BRAIN); DIFFUSION WEIGHTED IMAGING; ELECTRIC SHOCK; FEAR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENERALIZED ANXIETY DISORDER; GRAY MATTER; HUMAN; NERVOUS SYSTEM PARAMETERS; PRIORITY JOURNAL; RISK ASSESSMENT; TASK PERFORMANCE; TRACTOGRAPHY; VENTROMEDIAL PREFRONTAL CORTEX; WHITE MATTER;

ANXIETY; CONNECTIVITY; FEAR CONDITIONING; FEAR GENERALIZATON; RESTING-STATE; TRACTOGRAPHY;

ADOLESCENT; ADULT; ANXIETY DISORDERS; BRAIN MAPPING; CONDITIONING (PSYCHOLOGY); DIFFUSION TENSOR IMAGING; FEAR; FEMALE; GENERALIZATION (PSYCHOLOGY); HUMANS; LOGISTIC MODELS; MAGNETIC RESONANCE IMAGING; MODELS, NEUROLOGICAL; MULTIVARIATE ANALYSIS; PREFRONTAL CORTEX; YOUNG ADULT;

EID: 84896788738     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3372-13.2014     Document Type: Article

References (53)

1. Ayling E, Aghajani M, Fouche JP, van der Wee N (2012) Diffusion tensor imaging in anxiety disorders. Curr Psychiatry Rep 14:197-202. CrossRef Medline
2. Baas D, Aleman A, Kahn RS (2004) Lateralization of amygdala activation: a systematic review of functional neuroimaging studies. Brain Res Brain Res Rev 45:96-103. CrossRef Medline
3. Baumgartner T, Knoch D, Hotz P, Eisenegger C, Fehr E (2011) Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice. Nat Neurosci 14:1468-1474. CrossRef Medline
4. Behzadi Y, Restom K, Liau J, Liu TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37:90-101. CrossRef Medline
5. Bishop SJ (2009) Trait anxiety and impoverished prefrontal control of attention. Nat Neurosci 12:92-98. CrossRef Medline
6. Bishop S, Duncan J, Brett M, Lawrence AD (2004) Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli. Nat Neurosci 7:184-188. CrossRef Medline
7. Carlson JM, Cha J, Mujica-Parodi LR (2013a) Functional and structural amygdala-anterior cingulate connectivity correlates with attentional bias to masked fearful faces. Cortex 49:2595-2600. CrossRef Medline
8. Carlson JM, Cha J, Harmon-Jones E, Mujica-Parodi LR, Hajcak G (2013b) Influence of the BDNF genotype on amygdalo-prefrontal white matter microstructure is linked to nonconscious attention bias to threat. Cereb Cortex. Advance online publication. Retrieved February 13, 2014. Medline
9. Clark LA, Watson D (1991) Tripartite model of anxiety and depression: psychometric evidence and taxonomic implications. J Abnorm Psychol 100:316-336. CrossRef Medline
10. Cross L, Brown MW, Aggleton JP, Warburton EC (2012) The medial dorsal thalamic nucleus and the medial prefrontal cortex of the rat function together to support associative recognition and recency but not item recognition. Learn Mem 20:41-50. CrossRef Medline
11. Damasio AR (1996) The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philos Trans R Soc Lond B Biol Sci 351: 1413-1420. CrossRef Medline
12. Delgado MR, Nearing KI, Ledoux JE, Phelps EA (2008) Neural circuitry underlying the regulation of conditioned fear and its relation to extinction. Neuron 59:829-838. CrossRef Medline
13. Greenberg T, Carlson JM, Cha J, Hajcak G, Mujica-Parodi LR (2013a) Neural reactivity tracks fear generalization gradients. Biol Psychol 92:2-8. CrossRef Medline
14. Greenberg T, Carlson JM, Cha J, Hajcak G, Mujica-Parodi LR (2013b) Ventromedial prefrontal cortex reactivity is altered in generalized anxiety disorder during fear generalization. Depress Anxiety 30:242-250. CrossRef Medline
15. Hahn A, Stein P, Windischberger C, Weissenbacher A, Spindelegger C, Moser E, Kasper S, Lanzenberger R (2011) Reduced resting-state functional connectivity between amygdala and orbitofrontal cortex in social anxiety disorder. Neuroimage 56:881-889. CrossRef Medline
16. Hare TA, Camerer CF, Rangel A (2009) Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324:646-648. CrossRef Medline
17. Hartley CA, Fischl B, Phelps EA (2011) Brain structure correlates of individual differences in the acquisition and inhibition of conditioned fear. Cereb Cortex 21:1954-1962. CrossRef Medline
18. Heinz A, Braus DF, Smolka MN, Wrase J, Puls I, Hermann D, Klein S, Grüsser SM, Flor H, Schumann G, Mann K, Büchel C (2005) Amygdalaprefrontal coupling depends on a genetic variation of the serotonin transporter. Nat Neurosci 8:20-21. CrossRef Medline
19. Hettema JM, Kettenmann B, Ahluwalia V, McCarthy C, Kates WR, Schmitt JE, Silberg JL, Neale MC, Kendler KS, Fatouros P (2012) Pilot multimodal twin imaging study of generalized anxiety disorder. Depress Anxiety 29:202-209. CrossRef Medline
20. Hu LT, BentlerPM (1999) Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct Equ Modeling 6:1-55. CrossRef
21. Jennings JH, Sparta DR, Stamatakis AM, Ung RL, Pleil KE, Kash TL, Stuber GD (2013) Distinct extended amygdala circuits for divergent motivational states. Nature 496:224-228. CrossRef Medline
22. Kalisch R, Korenfeld E, Stephan KE, Weiskopf N, Seymour B, Dolan RJ (2006) Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. J Neurosci 26:9503-9511. CrossRef Medline
23. Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE (2005) Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62:593-602. CrossRef Medline
24. Kheirbek MA, Klemenhagen KC, Sahay A, Hen R (2012) Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci 15:1613-1620. CrossRef Medline
25. Kim MJ, Whalen PJ (2009) The structural integrity of an amygdalaprefrontal pathway predicts trait anxiety. J Neurosci 29:11614-11618. CrossRef Medline
26. Kim SY, Adhikari A, Lee SY, Marshel JH, Kim CK, Mallory CS, Lo M, Pak S, Mattis J, Lim BK, Malenka RC, Warden MR, Neve R, Tye KM, Deisseroth K (2013) Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 496:219-223. CrossRef Medline
27. Kriegeskorte N, Simmons WK, Bellgowan PS, Baker CI (2009) Circular analysis in systems neuroscience: the dangers of double dipping. Nat Neurosci 12:535-540. CrossRef Medline
28. Lee S, Ahmed T, Lee S, Kim H, Choi S, Kim DS, Kim SJ, Cho J, Shin HS (2012) Bidirectional modulation of fear extinction by mediodorsal thalamic firing in mice. Nat Neurosci 15:308-314. CrossRef Medline
29. Lehman JF, Greenberg BD, McIntyre CC, Rasmussen SA, Haber SN (2011) Rules ventral prefrontal cortical axons use to reach their targets: implications for diffusion tensor imaging tractography and deep brain stimulation for psychiatric illness. J Neurosci 31:10392-10402. CrossRef Medline
30. Lissek S (2012) Toward an account of clinical anxiety predicated on basic, neurally mapped mechanisms of Pavlovian fear-learning: the case for conditioned overgeneralization. Depress Anxiety 29:257-263. CrossRef Medline
31. Milad MR, Quirk GJ (2012) Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol 63:129-151. CrossRef Medline
32. Milad MR, Rauch SL (2007) The role of the orbitofrontal cortex in anxiety disorders. Ann N Y Acad Sci 1121:546-561. CrossRef Medline
33. Milad MR, Quinn BT, Pitman RK, Orr SP, Fischl B, Rauch SL (2005) Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. Proc Natl Acad Sci U S A 102:10706-10711. CrossRef Medline
34. Milad MR, Wright CI, Orr SP, Pitman RK, Quirk GJ, Rauch SL (2007) Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiat 62:446-454. CrossRef Medline
35. Mitchell AS, Gaffan D (2008) The magnocellular mediodorsal thalamus is necessary for memory acquisition, but not retrieval. J Neurosci 28:258-263. CrossRef Medline
36. Montag C, Reuter M, Weber B, Markett S, Schoene-Bake JC (2012) Individual differences in trait anxiety are associated with white matter tract integrity in the left temporal lobe in healthy males but not females. Neuroscience 217:77-83. CrossRef Medline
37. Myers-Schulz B, Koenigs M (2012) Functional anatomy of ventromedial prefrontal cortex: implications for mood and anxiety disorders. Mol Psychiatry 17:132-141. CrossRef Medline
38. O' Roak BJ, Deriziotis P, Lee C, Vives L, Schwartz JJ, Girirajan S, Karakoc E, Mackenzie AP, Ng SB, Baker C, Rieder MJ, Nickerson DA, Bernier R, Fisher SE, Shendure J, Eichler EE (2011) Exome sequencing in sporadic autism spectrum disorders identifies severe de novo mutations. Nat Genet 43:585-589. CrossRef Medline
39. Parnaudeau S, O'Neill PK, Bolkan SS, Ward RD, Abbas AI, Roth BL, Balsam PD, Gordon JA, Kellendonk C (2013) Inhibition of mediodorsal thalamus disrupts thalamofrontal connectivity and cognition. Neuron 77: 1151-1162. CrossRef Medline
40. Phan KL, Orlichenko A, Boyd E, Angstadt M, Coccaro EF, Liberzon I, Arfanakis K (2009) Preliminary evidence of white matter abnormality in the uncinate fasciculus in generalized social anxiety disorder. Biol Psychiat 66:691-694. CrossRef Medline
41. Phelps EA, Delgado MR, Nearing KI, LeDoux JE (2004) Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43:897-905. CrossRef Medline
42. Price JL (2007) Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann N Y Acad Sci 1121:54-71. CrossRef Medline
43. Robinson JL, Laird AR, Glahn DC, Lovallo WR, Fox PT (2010) Metaanalytic connectivity modeling: delineating the functional connectivity of the human amygdala. Hum Brain Mapp 31:173-184. CrossRef Medline
44. Roy M, Shohamy D, WagerTD (2012) Ventromedial prefrontal-subcortical systems and the generation of affective meaning. Trends Cogn Sci 16:147-156. CrossRef Medline
45. Schinka JA, Busch RM, Robichaux-Keene N (2004) A meta-analysis of the association between the serotonin transporter gene polymorphism (5-HTTLPR) and trait anxiety. Mol Psychiatry 9:197-202. CrossRef Medline
46. Sen S, Burmeister M, Ghosh D (2004) Meta-analysis of the association between a serotonin transporter promoter polymorphism (5-HTTLPR) and anxiety-related personality traits. Am J Med Genet B Neuropsychiatr Genet 127B:85-89. CrossRef Medline
47. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529-538. CrossRef Medline
48. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487-1505. CrossRef Medline
49. Sotres-Bayon F, Sierra-Mercado D, Pardilla-Delgado E, Quirk GJ (2012) Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron 76:804-812. CrossRef Medline
50. Spooner PM (2009) Sudden cardiac death: the larger problem. The larger genome. J Cardiovasc Electrophysiol 20:585-596. CrossRef Medline
51. Stein JL, Wiedholz LM, Bassett DS, Weinberger DR, Zink CF, Mattay VS, Meyer-Lindenberg A (2007) A validated network of effective amygdala connectivity. Neuroimage 36:736-745. CrossRef Medline
52. Tromp DP, Grupe DW, Oathes DJ, McFarlin DR, Hernandez PJ, Kral TR, Lee JE, Adams M, Alexander AL, Nitschke JB (2012) Reduced structural connectivity of a major frontolimbic pathway in generalized anxiety disorder. Arch Gen Psychiatry 69:925-934. CrossRef Medline
53. Yendiki A, Panneck P, Srinivasan P, Stevens A, Zöllei L, Augustinack J, Wang R, Salat D, Ehrlich S, Behrens T, Jbabdi S, Gollub R, Fischl B (2011) Automated probabilistic reconstruction of white-matter pathways in health and disease using an atlas of the underlying anatomy. Front Neuroinform 5:23. CrossRef Medline