Brain structure correlates of individual differences in the acquisition and inhibition of conditioned fear

Cerebral Cortex

Volumn 21, Issue 9, 2011, Pages 1954-1962

  Hartley, Catherine A ^a   Fischl, Bruce ^b,c   Phelps, Elizabeth A ^a  

^a NEW YORK UNIVERSITY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

cortical thickness; emotion regulation; fear conditioning; individual differences; insula

Indexed keywords

ADULT; ARTICLE; BRAIN REGION; BRAIN SIZE; CEREBROSPINAL FLUID; COGNITION; COMPARATIVE STUDY; CONDITIONING; CONTROLLED STUDY; ELECTRODE; ELECTRODERMAL RESPONSE; EMOTIONALITY; FEAR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; INSULA; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RADIOFREQUENCY; VENTROMEDIAL PREFRONTAL CORTEX;

ADOLESCENT; ADULT; BRAIN; BRAIN MAPPING; CEREBRAL CORTEX; CLUSTER ANALYSIS; COGNITION; CONDITIONING (PSYCHOLOGY); ELECTROSHOCK; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INDIVIDUALITY; MAGNETIC RESONANCE IMAGING; MALE; PHOTIC STIMULATION; YOUNG ADULT;

EID: 80051767643     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq253     Document Type: Article

References (79)

1. Barbas H. 2000. Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res Bull. 52:319-330. (Pubitemid 30462201)
2. Beauregard M, Levesque J, Bourgouin P. 2001. Neural correlates of conscious self-regulation of emotion. J Neurosci. 21:6993-7000.
3. Berns GS, Chappelow J, Cekic M, Zink CF, Pagnoni G, Martin-Skurski ME. 2006. Neurobiological substrates of dread. Science. 312:754-758.
4. Berry AC, Rosenfield D, Smits JAJ. 2009. Extinction retention predicts improvement in social anxiety symptoms following exposure therapy. Depression Anxiety. 26(1):22-27.
5. Bouton ME. 2004. Context and behavioral processes in extinction. Learn Mem. 11:485-494. (Pubitemid 39299694)
6. Brown CA, Seymour B, Boyle Y, El-Deredy W, Jones AK. 2007. Modulation of pain ratings by expectation and uncertainty: behavioral characteristics and anticipatory neural correlates. Pain. 135(3):240-250. (Pubitemid 351324023)
7. Bush DE, Sotres-Bayon F, Ledoux JE. 2007. Individual differences in fear: isolating fear reactivity and fear recovery phenotypes. J Trauma Stress. 20(4):413-422. (Pubitemid 47475492)
8. Craig AD. 2002. How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci. 3:655-666. (Pubitemid 135706673)
9. Critchley HD. 2002. Electrodermal responses: what happens in the brain. Neuroscientist. 8:132-142. (Pubitemid 34274074)
10. Critchley HD, Elliot R, Mathias CJ, Dolan RJ. 2000. Neural activity relating to the generation and representation of galvanic skin conductance response: a functional magnetic imaging study. J Neurosci. 20:3033-3040. (Pubitemid 30220328)
11. Critchley HD, Mathias CJ, Dolan RJ. 2002. Fear conditioning in humans: the influence of awareness and autonomic arousal on functional neuroanatomy. Neuron. 33:653-663. (Pubitemid 34188439)
12. Dale AM, Fischl B, Sereno MI. 1999. Cortical surface-based analysis I: segmentation and surface reconstruction. Neuroimage. 9(2):179-194. (Pubitemid 29369874)
13. Dale AM, Sereno MI. 1993. Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci. 5:162-176. (Pubitemid 23123842)
14. Dalton KM, Kalin NH, Grist TM, Davidson RJ. 2005. Neural-cardiac coupling in threat-evoked anxiety. J Cogn Neurosci. 17:969-980. (Pubitemid 40800029)
15. Davis M. 2000. The role of the amygdala in conditioned and unconditioned fear and anxiety. In: Aggleton JP, editor. The amygdala. Oxford: Oxford University Press. p. 213-288.
16. Delgado MR, Nearing KI, LeDoux JE, Phelps EA. 2008. Neural circuitry underlying the regulation of conditioned fear and its relation to extinction. Neuron. 59(5):829-838.
17. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, et al. 2006. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuro-image. 31(3):968-980. (Pubitemid 44183792)
18. Dickerson BC, Fenstermacher E, Salat DH, Wolk DA, Maguire RP, Desikan R, Pacheco J, Quinn BT, Van der Kouwe A, Greve DN, et al. 2008. Detection of cortical thickness correlates of cognitive performance: reliability across MRI scan sessions, scanners, and field strengths. Neuroimage. 39(1):10-18. (Pubitemid 350102218)
19. Dunsmoor JE, Knight DC, Bandettini PA. 2007. Impact of continuous versus intermittent CS-UCS pairing on human brain activation. Behav Neurosci. 121(4):635-642. (Pubitemid 47445118)
20. Dunsmoor JE, Schmajuk NA. 2009. Interpreting patterns of brain activation in human fear conditioning with an attentional-associative learning model. Behav Neurosci. 123(4):851-855.
21. Fendt M, Fanselow MS. 1999. The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev. 23:743-760. (Pubitemid 29282023)
22. Fischl B, Dale AM. 2000. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA. 97:11044-11049.
23. Fischl B, Liu A, Dale AM. 2001. Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging. 20(1):70-80. (Pubitemid 32293421)
24. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, et al. 2002. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 33:341-355. (Pubitemid 34162530)
25. Fischl B, Sereno M, Dale AM. 1999. Cortical surface-based analysis II: inflation, flattening, and surface-based coordinate system. Neuroimage. 9:195-207. (Pubitemid 29369875)
26. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat D, Busa E, Seidman L, Goldstein J, Kennedy D, et al. 2004. Automatically parcellating the human cerebral cortex. Cereb Cortex. 14:11-22. (Pubitemid 38018050)
27. Gianaros PJ, Sheu LK, Matthews KA, Jennings JR, Manuck SB, Hariri AR. 2008. Individual differences in stressor-evoked blood pressure reactivity vary with activation, volume, and functional connectivity of the amygdala. J Neurosci. 28(4):990-999. (Pubitemid 351159011)
28. Hartley CA, Phelps EA. 2010. Changing fear: the neurocircuitry of emotion regulation. Neuropsychopharmacology. 35(1):136-146.
29. Horton JC, Adams DL. 2005. The cortical column: a structure without a function. Philos Trans R Soc Lond B Biol Sci. 360:386-462.
30. Huettel SA, Song AW, McCarthy G. 2005. Decisions under uncertainty: probabilistic context influences activation of prefrontal and parietal cortices. J Neurosci. 25:3304-3311. (Pubitemid 40471339)
31. Jensen J, McIntosh AR, Crawley AP, Mikulis DJ, Remington G, Kapur S. 2003. Direct activation of the ventral striatum in anticipation of aversive stimuli. Neuron. 40:1251-1257. (Pubitemid 38032799)
32. Kimmel HD, Kimmel EB, Silver AI. 1969. The effect of UCS intensity in classical and avoidance GSR conditioning. Conditional Reflex. 4:32-51.
33. Knight DC, Smith CN, Cheng DT, Stein EA, Helmstetter FJ. 2004. Learning-related patterns of brain activation revealed using fMRI during acquisition and extinction of Pavlovian conditioned fear. Cogn Affect Behav Neurosci. 4:317-325.
34. Kuperberg GR, Broome MR, McGuire PK, David AS, Eddy M, Ozawa F, Goff D, West WC, Williams SC, van der Kouwe AJ, et al. 2003. Regionally localized thinning of the cerebral cortex in schizophrenia. Arch Gen Psychiatry. 60:878-888. (Pubitemid 37122306)
35. LaBar KS, Gatenby C, Gore JC, LeDoux JE, Phelps EA. 1998. Human amygdala activation during conditioned fear acquisition and extinction: a mixed trial fMRI study. Neuron. 20:937-945. (Pubitemid 28247399)
36. LeDoux JE. 2000. Emotion circuits in the brain. Annu Rev Neurosci. 23:155-184.
37. Maren S. 2001. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci. 24:897-931.
38. 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 USA. 102:10706-10711. (Pubitemid 41061618)
39. Milad MR, Quirk GJ. 2002. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature. 420:70-74. (Pubitemid 35291441)
40. Milad MR, Quirk GJ, Pitman RK, Orr SP, Fischl B, Rauch SL. 2007. A role for the human dorsal anterior cingulate cortex in fear expression. Biol Psychiatry. 62(10):1191-1194. (Pubitemid 350029727)
41. Milad MR, Orr SP, Lasko NB, Chang Y, Rauch SL, Pitman RK. 2008. Presence and acquired origin of reduced recall for fear extinction in PTSD: results of a twin study. J Psychiatr Res. 42:515-520.
42. Morgan MA, LeDoux JE. 1995. Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav Neurosci. 109:681-688.
43. Mountcastle VB. 1997. The columnar organization of the neocortex. Brain. 120(4):701-722. (Pubitemid 27174104)
44. Mugler JP, Brookeman JR. 1990. Three-dimensional magnetization-prepared rapid gradient-echo imaging (3D MP RAGE). Magn Reson Med. 15:152-157. (Pubitemid 20284023)
45. Ochsner KN, Gross JJ. 2005. The cognitive control of emotion. Trends Cogn Sci. 9(5):242-249. (Pubitemid 40615112)
46. Ochsner KN, Ray RD, Robertson ER, Cooper JC, Chopra S, Gabrieli JDE, Gross JJ. 2004. For better or for worse: neural systems supporting the cognitive down-and up-regulation of negative emotion. Neuroimage. 23(2):483-499. (Pubitemid 39370600)
47. Ongur D, Price JL. 2000. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex. 10:206-219. (Pubitemid 30159289)
48. Oppenheimer SM, Gelb A, Girvin JP, Hachinski VC. 1992. Cardiovascular effects of human insular cortex stimulation. Neurology. 42:1727-1732.
49. Ostrowsky K, Magnin M, Ryvlin P, Isnard J, Guenot M, Mauguiere F. 2002. Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. Cereb Cortex. 12:376-385. (Pubitemid 34226062)
50. Paulus MP, Stein MB. 2006. An insular view of anxiety. Biol Psychiatry. 60:383-387. (Pubitemid 44215849)
51. Peyron R, Laurent B, Garcia-Larrea L. 2000. Functional imaging of brain responses to pain. A review and meta-analysis. Neurophysiol Clin. 30:263-288.
52. Phelps EA, Delgado MR, Nearing KI, LeDoux JE. 2004. Extinction learning in humans: role of the amygdala and vmPFC. Neuron. 43(6):897-905. (Pubitemid 39215019)
53. Phelps EA, LeDoux JE. 2005. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron. 48:175-187. (Pubitemid 41476352)
54. Phelps EA, O'Connor KJ, Gatenby JC, Gore JC, Grillon C, Davis M. 2001. Activation of the left amygdala to a cognitive representation of fear. Nat Neurosci. 4:437-441. (Pubitemid 32260122)
55. Ploghaus A, Tracey I, Gati JS, Clare S, Menon RS, Matthews PM, Rawlins JN. 1999. Dissociating pain from its anticipation in the human brain. Science. 284:1979-1981. (Pubitemid 29309443)
56. Quirk GJ, Mueller D. 2008. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology. 33:56-72. (Pubitemid 350191313)
57. Rakic P. 1995. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 18:383-388.
58. Rauch SL, Shin LM, Phelps EA. 2006. Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroim-aging research-past, present, and future. Biol Psychiatry. 60: 376-382. (Pubitemid 44215857)
59. Rescorla RA, Wagner AR. 1972. A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforce-ment. In: Black AH, Prokasy WF, editors. Classical conditioning II. New York (NY): Appleton-Century-Crofts. p. 64-99.
60. Reynolds SM, Zahm DS. 2005. Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J Neurosci. 25:11757-11767. (Pubitemid 43098468)
61. Robinson CJ, Burton H. 1980. Somatic submodality distribution within the second somatosensory (SII), 7b, retroinsular, postauditory, and granular insular cortical areas of M. fascicularis. J Comp Neurol. 192:93-108. (Pubitemid 10039295)
62. Rosas HD, Liu AK, Hersch S, Glessner M, Ferrante RJ, Salat DH, van der Kouwe A, Jenkins BG, Dale AM, Fischl B. 2002. Regional and progressive thinning of the cortical ribbon in Huntington's disease. Neurology. 58:695-701. (Pubitemid 34211546)
63. Rosso IM, Killgore WD, Cintron CM, Gruber SA, Tohen M, Yurgelun-Todd DA. 2007. Reduced amygdala volumes in first-episode bipolar disorder and correlation with cerebral white matter. Biol Psychiatry. 61(6):743-749. (Pubitemid 46330244)
64. Sarinopoulos I, Grupe DW, Mackiewicz KL, Herrington JD, Lor M, Steege EE, Nitschke JB. 2010. Uncertainty during anticipation modulates neural responses to aversion in human insula and amygdala. Cereb Cortex. 20(4):929-940.
65. Schlosberg H, Stanley WC. 1953. A simple test of the normality of twenty-four distributions of electrical skin conductance. Science. 117:35-37.
66. Schultz W, Dayan P, Montague PR. 1997. A neural substrate of prediction and reward. Science. 275:1593-1599. (Pubitemid 27120526)
67. Shi C, Davis M. 1999. Pain pathways involved in fear conditioning measured with fear-potentiated startle: lesion studies. J Neurosci. 19:420-430. (Pubitemid 29028981)
68. Silver AI, McCaffrey RJ, Godfrey G. 1978. Effects of UCS intensity and postpeak acquisition trials on classical conditioning of the SCR. Acta Psychol. 42(3):225-230.
69. Simmons A, Strigo I, Matthews SC, Paulus MP, Stein MB. 2006. Anticipation of aversive visual stimuli is associated with increased insula activation in anxiety-prone subjects. Biol Psychiatry. 60(4):402-409. (Pubitemid 44215851)
70. Sotres-Bayon F, Cain CK, LeDoux JE. 2006. Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biol Psychiatry. 60:329-336. (Pubitemid 44215846)
71. Szeszko PR, Robinson D, Alvir JM, Bilder RM, Lencz T, Ashtari M, Wu H, Bogerts B. 1999. Orbital frontal and amygdala volume reductions in obsessive-compulsive disorder. Arch Gen Psychiatry. 56(10): 913-919. (Pubitemid 29480127)
72. Talairach J, Tournoux P. 1988. Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system-an approach to cerebral imaging. New York: Thieme Medical.
73. Urry HL, van Reekum CM, Johnstone T, Kalin NH, Thurow ME, Schaefer HS, Jackson CA, Frye CJ, Greischar LL, Alexander AL, et al. 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. J Neurosci. 26: 4415-4425. (Pubitemid 44315400)
74. Vidal-Gonzalez I, Vidal-Gonzalez B, Rauch SL, Quirk GJ. 2006. Micro-stimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem. 13:728-733. (Pubitemid 44871673)
75. Wager TD, Davidson ML, Hughes BL, Lindquist MA, Ochsner KN. 2008. Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron. 59:1037-1050.
76. Wager TD, Rilling JK, Smith EE, Sokolik A, Casey KL, Davidson RJ, Rose RM, Cohen JD. 2004. Placebo-induced changes in FMRI in the anticipation and experience of pain. Science. 303:1162-1167. (Pubitemid 38233575)
77. Worsley KJ, Taylor JE, Carbonell F, Chung MK, Duerden E, Bernhardt B, Lyttelton O, Boucher M, Evans AC. 2009. SurfStat: a Matlab toolbox for the statistical analysis of univariate and multivariate surface and volumetric data using linear mixed effects models and random field theory. Proceedings of the 15th Annual Meeting of the Organization for Human Brain Mapping. San Francisco (CA): Neuroimage.
78. Yang RJ, Mozhui K, Karlsson RM, Cameron HA, Williams RW, Holmes A. 2008. Variation in mouse basolateral amygdala volume is associated with differences in stress reactivity and fear learning. Neuro-psychopharmacology. 33(11):2595-2604.
79. Zetzsche T, Frodl T, Preuss UW, Schmitt G, Seifert D, Leinsinger G, Born C, Reiser M, Moller HJ, Meisenzahl EM. 2006. Amygdala volume and depressive symptoms in patients with borderline personality disorder. Biol Psychiatry. 60(3):302-310. (Pubitemid 44093445)