Brain morphology correlates of interindividual differences in conditioned fear acquisition and extinction learning

Brain Structure and Function

Volumn 221, Issue 4, 2016, Pages 1927-1937

  Winkelmann, Tobias ^a   Grimm, Oliver ^a   Pohlack, Sebastian T ^a   Nees, Frauke ^a   Cacciaglia, Raffaele ^a   Dinu Biringer, Ramona ^a   Steiger, Frauke ^a   Wicking, Manon ^a   Ruttorf, Michaela ^a   Schad, Lothar R ^a   Flor, Herta ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Amygdala; Brain structure; Cortical thickness; Extinction learning; Fear conditioning; vmPFC

Indexed keywords

AMYGDALA; ARTICLE; BRAIN; CONDITIONING; CONTROLLED STUDY; ELECTRODERMAL RESPONSE; EXTINCTION LEARNING; FEAR; HUMAN; LEARNING; MAJOR CLINICAL STUDY; MORPHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; VENTROMEDIAL PREFRONTAL CORTEX; ADULT; ANATOMY AND HISTOLOGY; CONDITIONED REFLEX; FEMALE; INDIVIDUALITY; MALE; PHYSIOLOGY; PREFRONTAL CORTEX; REINFORCEMENT; YOUNG ADULT;

ADULT; AMYGDALA; BRAIN; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; GALVANIC SKIN RESPONSE; HUMANS; INDIVIDUALITY; MAGNETIC RESONANCE IMAGING; MALE; PREFRONTAL CORTEX; YOUNG ADULT;

EID: 84923601520     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-015-1013-z     Document Type: Article

References (67)

1. Amano T, Unal CT, Pare D (2010) Synaptic correlates of fear extinction in the amygdala. Nat Neurosci 13:489–494
2. Anders S, Lotze M, Wildgruber D, Erb M, Grodd W, Birbaumer N (2005) Processing of a simple aversive conditioned stimulus in a divided visual field paradigm: an fMRI study. Exp Brain Res 162:213–219
3. Barnes J et al (2010) Head size, age and gender adjustment in MRI studies: a necessary nuisance? Neuroimage 53:1244–1255
4. Barrett J, Armony JL (2009) Influence of trait anxiety on brain activity during the acquisition and extinction of aversive conditioning. Psychol Med 39:255–265
5. Baur V, Hanggi J, Jancke L (2012) Volumetric associations between uncinate fasciculus, amygdala, and trait anxiety. BMC Neurosci 13:4
6. Benedek M, Kaernbach C (2010a) A continuous measure of phasic electrodermal activity. J Neurosci Methods 190:80–91
7. Benedek M, Kaernbach C (2010b) Decomposition of skin conductance data by means of non-negative deconvolution. Psychophysiology 47:647–658
8. Blackmon K et al (2011) Structural evidence for involvement of a left amygdala-orbitofrontal network in subclinical anxiety. Psychiatry Res 194:296–303
9. Boucsein W, Fowles DC, Grimnes S, Ben-Shakhar G, Roth WT, Dawson ME, Filion DL (2012) Publication recommendations for electrodermal measurements. Psychophysiology 49:1017–1034
10. Bradley MM, Lang PJ (1994) Measuring emotion: the self-assessment manikin and the semantic differential. J Behav Ther Exp Psychiatry 25:49–59
11. Büchel C, Morris J, Dolan RJ, Friston KJ (1998) Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron 20:947–957
12. Cacciaglia R et al (2013) A risk variant for alcoholism in the NMDA receptor affects amygdala activity during fear conditioning in humans. Biol Psychol 94:74–81
13. Cacciaglia R, Pohlack ST, Flor H, Nees F (2014) Dissociable roles for hippocampal and amygdalar volume in human fear conditioning. Brain Struct Funct. doi:10.1007/s00429-014-0807-8
14. Chang CH, Berke JD, Maren S (2010) Single-unit activity in the medial prefrontal cortex during immediate and delayed extinction of fear in rats. PLoS One 5:e11971
15. Cheng DT, Knight DC, Smith CN, Helmstetter FJ (2006) Human amygdala activity during the expression of fear responses. Behav Neurosci 120:1187–1195
16. Chung MK, Worsley KJ, Nacewicz BM, Dalton KM, Davidson RJ (2010) General multivariate linear modeling of surface shapes using SurfStat. Neuroimage 53:491–505
17. Ciocchi S et al (2010) Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468:277–282
18. Corcoran KA, Quirk GJ (2007) Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J Neurosci 27:840–844
19. Coupe P, Yger P, Barillot C (2006) Fast non local means denoising for 3D MR images. Med Image Comput Comput Assist Interv 9:33–40
20. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194
21. Derix J et al (2014) Visualization of the amygdalo-hippocampal border and its structural variability by 7T and 3T magnetic resonance imaging. Hum Brain Mapp 35:4316–4329
22. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055
23. Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207
24. Garcia R, Chang CH, Maren S (2006) Electrolytic lesions of the medial prefrontal cortex do not interfere with long-term memory of extinction of conditioned fear. Learn Mem 13:14–17
25. Gazendam FJ, Kamphuis JH, Kindt M (2013) Deficient safety learning characterizes high trait anxious individuals. Biol Psychol 92:342–352
26. Gottfried JA, Dolan RJ (2004) Human orbitofrontal cortex mediates extinction learning while accessing conditioned representations of value. Nat Neurosci 7:1144–1152
27. Haaker J, Lonsdorf TB, Thanellou A, Kalisch R (2013) Multimodal assessment of long-term memory recall and reinstatement in a combined cue and context fear conditioning and extinction paradigm in humans. PLoS One 8:e76179. doi:10.1371/journal.pone.0076179
28. Han X et al (2006) Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. Neuroimage 32:180–194
29. 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
30. Jovanovic T et al (2012) Reduced neural activation during an inhibition task is associated with impaired fear inhibition in a traumatized civilian sample. Cortex 49:1884–1891
31. Kanai R, Rees G (2011) The structural basis of inter-individual differences in human behaviour and cognition. Nat Rev Neurosci 12:231–242
32. Knight DC, Waters NS, Bandettini PA (2009) Neural substrates of explicit and implicit fear memory. Neuroimage 45:208–214
33. Konorsky J (1967) Integrative Activity of the Brain. University of Chicago Press, Chicago
34. Kuperberg GR et al (2003) Regionally localized thinning of the cerebral cortex in schizophrenia. Arch Gen Psychiatry 60:878–888
35. LaBar KS, Gatenby JC, 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
36. Laux L, Glanzmann P, Schaffner P, Spielberger CD (1981) Das State-Trait-Angstinventar (STAI). Beltz-Testgesellschaft, Weinheim, Germany
37. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184
38. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM (1990) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10:1062–1069
39. Lykken DT, Venables PH (1971) Direct measurement of skin conductance: a proposal for standardization. Psychophysiology 8:656–672
40. Maren S, Quirk GJ (2004) Neuronal signalling of fear memory. Nat Rev Neurosci 5:844–852
41. Meulders A, Meulders M, Vlaeyen JW (2014) Positive affect protects against deficient safety learning during extinction of fear of movement-related pain in healthy individuals scoring relatively high on trait anxiety. J Pain 15:632–644
42. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70–74
43. Milad MR, Quirk GJ (2012) Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol 63:129–151
44. Milad MR, Vidal-Gonzalez I, Quirk GJ (2004) Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner. Behav Neurosci 118:389–394
45. 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
46. Milad MR, Quirk GJ, Pitman RK, Orr SP, Fischl B, Rauch SL (2007a) A role for the human dorsal anterior cingulate cortex in fear expression. Biol Psychiatry 62:1191–1194
47. Milad MR, Wright CI, Orr SP, Pitman RK, Quirk GJ, Rauch SL (2007b) Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiatry 62:446–454
48. Morgan MA, Romanski LM, LeDoux JE (1993) Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Lett 163:109–113
49. 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
50. Pape HC, Pare D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90:419–463
51. Pavlov IP (1927) Conditioned reflexes. Oxford University Press, London
52. 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
53. Pineles SL, Orr MR, Orr SP (2009) An alternative scoring method for skin conductance responding in a differential fear conditioning paradigm with a long-duration conditioned stimulus. Psychophysiology 46:984–995
54. Pohlack ST, Nees F, Ruttorf M, Witt SH, Nieratschker V, Rietschel M, Flor H (2011) Risk variant for schizophrenia in the neurogranin gene impacts on hippocampus activation during contextual fear conditioning. Mol Psychiatry 16:1072–1073
55. Quirk GJ, Mueller D (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33:56–72
56. Quirk GJ, Russo GK, Barron JL, Lebron K (2000) The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J Neurosci 20:6225–6231
57. Ridder S et al (2012) Brain activation during fear conditioning in humans depends on genetic variations related to functioning of the hypothalamic-pituitary-adrenal axis: first evidence from two independent subsamples. Psychol Med 42:2325–2335
58. Rosas HD, Hevelone ND, Zaleta AK, Greve DN, Salat DH, Fischl B (2005) Regional cortical thinning in preclinical Huntington disease and its relationship to cognition. Neurology 65:745–747
59. Sehlmeyer C, Schoning S, Zwitserlood P, Pfleiderer B, Kircher T, Arolt V, Konrad C (2009) Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS One 4:e5865
60. 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
61. Striedter GF (2005) Principles of brain evolution. Sinauer Associates, Sunderland
62. Torrents-Rodas D, Fullana MA, Bonillo A, Caseras X, Andion O, Torrubia R (2013) No effect of trait anxiety on differential fear conditioning or fear generalization. Biol Psychol 92:185–190
63. van Well S, Visser RM, Scholte HS, Kindt M (2012) Neural substrates of individual differences in human fear learning: evidence from concurrent fMRI, fear-potentiated startle, and US-expectancy data. Cogn Affect Behav Neurosci 12:499–512
64. Venables PH, Christie MJ (1980) Electrodermal activity. In: Martin I, Venables PH (eds) Techniques in psychophysiology. John Wiley, New York, pp 2–67
65. Wittchen HU, Wunderlich U, Gruschwitz S, Zaudig M (1997) SKID-I. Strukturiertes Klinisches Interview für DSM-IV. Hogrefe, Göttingen
66. 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. In: Proceedings of the 15th annual meeting of the organization for human brain mapping, San Francisco, California, June 2009
67. Zeidan MA et al (2011) Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biol Psychiatry 70:920–927