Exposure to subliminal arousing stimuli induces robust activation in the amygdala, hippocampus, anterior cingulate, insular cortex and primary visual cortex: A systematic meta-analysis of fMRI studies

NeuroImage

Volumn 59, Issue 3, 2012, Pages 2962-2973

  Brooks, S J ^a   Savov, V ^a   Allzen E ^a   Benedict, C ^a   Fredriksson, R ^a   Schioth H B ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Audio; Emotional faces; FMRI; Meta analysis; Motivation; Physiological; Subliminal; Words

Indexed keywords

AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; AROUSAL; AUDITORY STIMULATION; CONFLICT; EMOTION; FACIAL EXPRESSION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; IMPLICIT MEMORY; INSULA; MENTAL DISEASE; PHOBIA; PRIORITY JOURNAL; REVIEW; SOMATOSENSORY STIMULATION; STIMULUS RESPONSE; STRIATE CORTEX; WORD RECOGNITION;

ACOUSTIC STIMULATION; AMYGDALA; AROUSAL; CEREBRAL CORTEX; GYRUS CINGULI; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; PHOTIC STIMULATION; SUBLIMINAL STIMULATION; VISUAL CORTEX;

EID: 84855436269     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.09.077     Document Type: Review

References (81)

1. Andresen V., et al. Brain activation responses to subliminal or supraliminal rectal stimuli and to auditory stimuli in irritable bowel syndrome. Neurogastroenterol. Motil. 2005, 17:827-837.
2. Banse R., Seise J., Zerbes N. Implicit attitudes towards homosexuality: reliability, validity, and controllability of the IAT. Z. Exp. Psychol. 2001, 48:145-160.
3. Bennett C.M., Miller M.B. How reliable are the results from functional magnetic resonance imaging?. Ann. N. Y. Acad. Sci. 2010, 1191:133-155.
4. Bianchi-Demicheli F., Ortigue S. Mental representation of subjective pleasure of partnered experiences in women's brain conveyed through event-related fMRI. Med. Sci. Monit. 2009, 15:CR545-CR550.
5. Bijsterbosch J.D., et al. The role of the cerebellum in sub- and supraliminal error correction during sensorimotor synchronization: evidence from fMRI and TMS. J. Cogn. Neurosci. 2011, 23:1100-1112.
6. Botvinick M.M. Conflict monitoring and decision making: reconciling two perspectives on anterior cingulate function. Cogn. Affect Behav. Neurosci. 2007, 7(4):356-366.
7. Conty, L., Grezes, J., in press. Look at me, I'll remember you: the perception of self-relevant social cues enhances memory and right hippocampal activity. Hum. Brain Mapp.
8. Costafreda S.G., et al. Predictors of amygdala activation during the processing of emotional stimuli: a meta-analysis of 385 PET and fMRI studies. Brain Res. Rev. 2008, 58:57-70.
9. Craig A.D. How do you feel-now? The anterior insula and human awareness. Nat. Rev. Neurosci. 2009, 10:59-70.
10. Craig A.D. Significance of the insula for the evolution of human awareness of feelings from the body. Ann. N. Y. Acad. Sci. 2011, 1225:72-82.
11. Critchley H.D., et al. Neural systems supporting interoceptive awareness. Nat. Neurosci. 2004, 7:189-195.
12. Cowell R.A., Bussey T.J., Saksida L.M. Components of recognition memory: dissociable cognitive processes or just differences in representational complexity?. Hippocampus 2010, 20(11):1245-1262.
13. Damasio A. The Self Comes to Mind: Constructing the Conscious Brain 2010, Vol., Pantheon Books, New York.
14. Dannlowski U., et al. Amygdala reactivity predicts automatic negative evaluations for facial emotions. Psychiatry Res. 2007, 154:13-20.
15. Degonda N., et al. Implicit associative learning engages the hippocampus and interacts with explicit associative learning. Neuron 2005, 46:505-520.
16. Dehaene S., et al. Conscious and subliminal conflicts in normal subjects and patients with schizophrenia: the role of the anterior cingulate. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13722-13727.
17. Dehaene S., et al. Letter binding and invariant recognition of masked words: behavioral and neuroimaging evidence. Psychol. Sci. 2004, 15:307-313.
18. Dehaene S., et al. Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends Cogn. Sci. 2006, 10:204-211.
19. Diaz M.T., McCarthy G. Unconscious word processing engages a distributed network of brain regions. J. Cogn. Neurosci. 2007, 19:1768-1775.
20. Diekhof E.K., et al. Top-down and bottom-up modulation of brain structures involved in auditory discrimination. Brain Res. 2009, 1297:118-123.
21. Duan X., et al. Neural mechanism of unconscious perception of surprised facial expression. Neuroimage 2010, 52:401-407.
22. Dunsmoor J.E., et al. Neurobehavioral mechanisms of human fear generalization. Neuroimage 2011, 55:1878-1888.
23. Eickhoff S.B., et al. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum. Brain Mapp. 2009, 30:2907-2926.
24. Eickhoff S.B., Nickl-Jockschat T., Kurth F. Meta-analyses in clinical brain research. Nervenarzt 2010, 81:32-38.
25. Fazio R.H., Olson M.A. Implicit measures in social cognition. research: their meaning and use. Annu. Rev. Psychol. 2003, 54:297-327.
26. Gray J.R. Emotional modulation of cognitive control: approach-withdrawal states double-dissociate spatial from verbal two-back task performance. J. Exp. Psychol. Gen. 2001, 130:436-452.
27. Hartikainen K.M., Ogawa K.H., Knight R.T. Transient interference of right hemispheric function due to automatic emotional processing. Neuropsychologia 2000, 38:1576-1580.
28. Heinzel A., et al. Neural correlates of subliminal and supraliminal letter processing-an event-related fMRI study. Conscious. Cogn. 2008, 17:685-699.
29. Janzen G., Weststeijn C.G. Neural representation of object location and route direction: an event-related fMRI study. Brain Res. 2007, 1165:116-125.
30. Kanwisher N., Yovel G. The fusiform face area: a cortical region specialised for the perception of faces. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2006, 361(1476):2109-2128.
31. Kern M., et al. Characterization of the cerebral cortical representation of heartburn in GERD patients. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 286:G174-G181.
32. Killgore W.D., Yurgelun-Todd D.A. Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces. Neuroimage 2004, 21:1215-1223.
33. Kim C., Chung C., Kim J. Multiple cognitive control mechanisms associated with the nature of conflict. Neurosci. Lett. 2010, 476(3):156-160.
34. Kouider S., Dehaene S. Levels of processing during non-conscious perception: a critical review of visual masking. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2007, 362:857-875.
35. Kouider S., et al. Cerebral bases of subliminal and supraliminal priming during reading. Cerebral Cortex 2007, 17:2019-2029.
36. Kouider S., et al. Activity in face-responsive brain regions is modulated by invisible, attended faces: evidence from masked priming. Cereb. Cortex 2009, 19:13-23.
37. Kouider S., et al. Cerebral bases of subliminal speech priming. Neuroimage 2010, 49:922-929.
38. Laird A.R., et al. ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Hum. Brain Mapp. 2005, 25:155-164.
39. Lawal A., et al. Cingulate cortex: a closer look at its gut-related functional topography. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 289:G722-G730.
40. Lawal A., et al. Novel evidence for hypersensitivity of visceral sensory neural circuitry in irritable bowel syndrome patients. Gastroenterology 2006, 130:26-33.
41. Lawal A., et al. Neurocognitive processsing of esophageal central sensitization in the insula and cingulate gyrus. Am J. Physiological Gastrointestinal Liver Physiology 2008, 294:G787-G794.
42. LeDoux, J., 1996. The Emotional Brain: The Mysterious Underpinnings of Emotional Life. Vol., ed.^eds. First Touchstone Edition, New York.
43. LeDoux J. The emotional brain, fear, and the amygdala. Cell. Mol. Neurobiol. 2003, 23:727-738.
44. Liddell B.J., et al. A direct brainstem-amygdala-cortical 'alarm' system for subliminal signals of fear. Neuroimage 2005, 24:235-243.
45. Lipka J., Miltner W.H., Straube T. Vigilance for threat interacts with amygdala responses to subliminal threat cues in specific phobia. Biol. Psychiatry 2011, 70:472-478.
46. Litt A., et al. Dissociating valuation and saliency signals during decision-making. Cereb. Cortex 2011, 21:95-102.
47. Luo Q., et al. Emotional valence of words modulates the subliminal repetition priming effect in the left fusiform gyrus: an event-related fMRI study. Neuroimage 2004, 21:414-421.
48. Morris J.P., Pelphrey K.A., McCarthy G. Face processing without awareness in the right fusiform gyrus. Neuropsychologia 2007, 45:3087-3091.
49. Murphy S.T., Zajonc R.B. Affect, cognition, and awareness: affective priming with optimal and suboptimal stimulus exposures. J. Pers. Soc. Psychol. 1993, 64:723-739.
50. Naccache L., Dehaene S. The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. Cereb. Cortex 2001, 11:966-974.
51. Naccache L., et al. A direct intracranial record of emotions evoked by subliminal words. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:7713-7717.
52. Nakamura K., et al. Subliminal convergence of Kanji and Kana words: further evidence for functional parcellation of the posterior temporal cortex in visual word perception. J. Cogn. Neurosci. 2005, 17:954-968.
53. Nakamura K., et al. Task-specific change of unconscious neural priming in the cerebral language network. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:19643-19648.
54. Nomura M., et al. Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study. Neuroimage 2004, 21:352-363.
55. Ortigue S., et al. The Neural Basis of Love as a Subliminal Prime: An Event-related Functional Magnetic Resonance Imaging Study. Journal of Cognitive Neuroscience 2007, 19(7):1218-1230.
56. Ortigue S., Grafton S.T., Bianchi-Demicheli F. Correlation between insula activation and self-reported quality of orgasm in women. Neuroimage 2007, 37:551-560.
57. Ortigue S., et al. Neuroimaging of love: fMRI meta-analysis evidence toward new perspectives in sexual medicine. J. Sex. Med. 2010, 7:3541-3552.
58. Pannese A., Hirsch J. Self-face enhances processing of immediately preceding invisible faces. Neuropsychologia 2011, 49:564-573.
59. Paus T. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat. Rev. Neurosicence 2001, 2(6):417-424.
60. Pessiglione M., et al. How the brain translates money into force: a neuroimaging study of subliminal motivation. Science 2007, 316:904-906.
61. Pessiglione M., et al. Subliminal instrumental conditioning demonstrated in the human brain. Neuron 2008, 59:561-567.
62. Phillips M.L., et al. Differential neural responses to overt and covert presentations of facial expressions of fear and disgust. Neuroimage 2004, 21:1484-1496.
63. Qiao E., et al. Unconsciously deciphering handwriting: subliminal invariance for handwritten words in the visual word form area. Neuroimage 2010, 49:1786-1799.
64. Sabatini E., et al. Brain structures activated by overt and covert emotional visual stimuli. Brain Res. Bull. 2009, 79:258-264.
65. Said C.P., Haxby J.V., Todorov A. Brain systems for assessing the affective value of faces. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2011, 366:1660-1670.
66. Shelley B.P., Trimble M.R. The insular lobe of Reil - its anatamico-functional, behavioural and neuropsychiatric attributes in humans - a review. World J. Biol. Psychiatry 2004, 5:176-200.
67. Sidhu H., Kern M., Shaker R. Absence of increasing cortical fMRI activity volume in response to increasing visceral stimulation in IBS patients. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 287:G425-G435.
68. Smith J.K., et al. fMRI and MEG analysis of visceral pain in healthy volunteers. Neurogastroenterol. Motil. 2011, 23:648-e260.
69. Squire L.R., Wixted J.T. The cognitive neuroscience of human memory since H.M. Annu. Rev. Neurosci. 2011, 34:259-288.
70. Straube T., et al. Dynamic activation of the anterior cingulate cortex during anticipatory anxiety. Neuroimage 2009, 44:975-981.
71. Suslow T., et al. Automatic mood-congruent amygdala responses to masked facial expressions in major depression. Biol. Psychiatry 2010, 67:155-160.
72. Taskin B., et al. Inhibitory impact of subliminal electrical finger stimulation on SI representation and perceptual sensitivity of an adjacent finger. NeuroImage 2008, 39:1307-1313.
73. Talairach J., Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain: Translated by Mark Rayport 1988, Vol., Thieme Classics.
74. Tillisch K., Mayer E.A., Labus J.S. Quantitative meta-analysis identifies brain regions activated during rectal distension in irritable bowel syndrome. Gastroenterology 2011, 140:91-100.
75. Turkeltaub, P.E., et al., in press. Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum. Brain Mapp.
76. Van der Laan L.N., de Ridder D.T., Viergever M.A., Smeets P.A. The first taste is always with the eyes: a meta-analysis on the neural correlates of processing visual food cues. Neuroimage 2011, 55:296-303.
77. Vizueta N., et al. Dispositional fear, negative affectivity, and neuroimaging response to visually suppressed emotional faces. Neuroimage 2012, 59:761-771.
78. Wiener M., Turkeltaub P., Coslett H.B. The image of time: a voxel-wise meta-analysis. Neuroimage 2010, 49(2):1728-1740.
79. Williams L.M., et al. Amygdala-prefrontal dissociation of subliminal and supraliminal fear. Hum. Brain Mapp. 2006, 27:652-661.
80. Wolbers T., et al. Changes in connectivity profiles as a mechanism for strategic control over interfering subliminal information. Cereb. Cortex 2006, 16:857-864.
81. Yeung N., Nieuwenhuis S. Dissociating response conflict and error likelihood in anterior cingulate cortex. J. Neurosci. 2009, 29(46):14506-14510.