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

Functional Magnetic Resonance Imaging (fMRI) demonstrates that the subliminal presentation of arousing stimuli can activate subcortical brain regions independently of consciousness-generating top-down cortical modulation loops. Delineating these processes may elucidate mechanisms for arousal, aberration in which may underlie some psychiatric conditions. Here we are the first to review and discuss four Activation Likelihood Estimation (ALE) meta-analyses of fMRI studies using subliminal paradigms. We find a maximum of 9 out of 12 studies using subliminal presentation of faces contributing to activation of the amygdala, and also a significantly high number of studies reporting activation in the bilateral anterior cingulate, bilateral insular cortex, hippocampus and primary visual cortex. Subliminal faces are the strongest modality, whereas lexical stimuli are the weakest. Meta-analyses independent of studies using Regions of Interest (ROI) revealed no biasing effect. Core neuronal arousal in the brain, which may be at first independent of conscious processing, potentially involves a network incorporating primary visual areas, somatosensory, implicit memory and conflict monitoring regions. These data could provide candidate brain regions for the study of psychiatric disorders associated with aberrant automatic emotional processing.

[1]  S. Nieuwenhuis,et al.  Dissociating Response Conflict and Error Likelihood in Anterior Cingulate Cortex , 2009, The Journal of Neuroscience.

[2]  Joseph E LeDoux.  The Emotional Brain, Fear, and the Amygdala , 2003, Cellular and Molecular Neurobiology.

[3]  Andrzej Jesmanowicz,et al.  Neurocognitive processing of esophageal central sensitization in the insula and cingulate gyrus. , 2008, American journal of physiology. Gastrointestinal and liver physiology.

[4]  Max A. Viergever,et al.  The first taste is always with the eyes: A meta-analysis on the neural correlates of processing visual food cues , 2011, NeuroImage.

[5]  Gian Luca Romani,et al.  Brain structures activated by overt and covert emotional visual stimuli , 2009, Brain Research Bulletin.

[6]  Qian Luo,et al.  Emotional valence of words modulates the subliminal repetition priming effect in the left fusiform gyrus: an event-related fMRI study , 2004, NeuroImage.

[7]  Leanne M Williams,et al.  Amygdala–prefrontal dissociation of subliminal and supraliminal fear , 2006, Human brain mapping.

[8]  R. Dolan,et al.  How the Brain Translates Money into Force: A Neuroimaging Study of Subliminal Motivation , 2007, Science.

[9]  Simon B Eickhoff,et al.  Minimizing within‐experiment and within‐group effects in activation likelihood estimation meta‐analyses , 2012, Human brain mapping.

[10]  R. Knight,et al.  Transient interference of right hemispheric function due to automatic emotional processing , 2000, Neuropsychologia.

[11]  M. Trimble,et al.  The insular Lobe of Reil–its Anatamico-Functional, behavioural and Neuropsychiatric attributes in humans–a review , 2004, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[12]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[13]  A. David,et al.  Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies , 2008, Brain Research Reviews.

[14]  Walter Heindel,et al.  Amygdala reactivity predicts automatic negative evaluations for facial emotions , 2007, Psychiatry Research: Neuroimaging.

[15]  Kirsten Tillisch,et al.  Quantitative meta-analysis identifies brain regions activated during rectal distension in irritable bowel syndrome. , 2011, Gastroenterology.

[16]  Harjot Sidhu,et al.  Novel evidence for hypersensitivity of visceral sensory neural circuitry in irritable bowel syndrome patients. , 2006, Gastroenterology.

[17]  Kevin A. Pelphrey,et al.  Face processing without awareness in the right fusiform gyrus , 2007, Neuropsychologia.

[18]  Stanislas Dehaene,et al.  Subliminal Convergence of Kanji and Kana Words: Further Evidence for Functional Parcellation of the Posterior Temporal Cortex in Visual Word Perception , 2005, Journal of Cognitive Neuroscience.

[19]  Christopher Andrew,et al.  Differential neural responses to overt and covert presentations of facial expressions of fear and disgust , 2000, NeuroImage.

[21]  Stephanie Ortigue,et al.  Mental representation of subjective pleasure of partnered experiences in women's brain conveyed through event-related fMRI. , 2009, Medical science monitor : international medical journal of experimental and clinical research.

[22]  Oliver Gruber,et al.  Top-down and bottom-up modulation of brain structures involved in auditory discrimination , 2009, Brain Research.

[23]  Stephanie Ortigue,et al.  Neuroimaging of love: fMRI meta-analysis evidence toward new perspectives in sexual medicine. , 2010, The journal of sexual medicine.

[24]  L. Squire,et al.  The cognitive neuroscience of human memory since H.M. , 2011, Annual review of neuroscience.

[25]  Thomas Straube,et al.  Vigilance for Threat Interacts with Amygdala Responses to Subliminal Threat Cues in Specific Phobia , 2011, Biological Psychiatry.

[26]  R. Banse,et al.  Implicit attitudes towards homosexuality: reliability, validity, and controllability of the IAT. , 2001, Zeitschrift fur experimentelle Psychologie : Organ der Deutschen Gesellschaft fur Psychologie.

[27]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[28]  Pienie Zwitserlood,et al.  Automatic Mood-Congruent Amygdala Responses to Masked Facial Expressions in Major Depression , 2010, Biological Psychiatry.

[29]  Richard N. Henson,et al.  Activity in Face-Responsive Brain Regions is Modulated by Invisible, Attended Faces: Evidence from Masked Priming , 2008, Cerebral cortex.

[30]  Vishnu P. Murty,et al.  Neurobehavioral mechanisms of human fear generalization , 2011, NeuroImage.

[31]  Reza Shaker,et al.  Characterization of the cerebral cortical representation of heartburn in GERD patients. , 2004, American journal of physiology. Gastrointestinal and liver physiology.

[32]  S B Eickhoff,et al.  [Meta-analyses in clinical brain research]. , 2010, Der Nervenarzt.

[33]  Arno Villringer,et al.  Inhibitory impact of subliminal electrical finger stimulation on SI representation and perceptual sensitivity of an adjacent finger , 2008, NeuroImage.

[34]  F. Boers,et al.  Neural correlates of subliminal and supraliminal letter processing—An event-related fMRI study , 2008, Consciousness and Cognition.

[35]  Alexander Todorov,et al.  Brain systems for assessing the affective value of faces , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[36]  S. Dehaene,et al.  Levels of processing during non-conscious perception: a critical review of visual masking , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  Michael D. Hunter,et al.  The Role of the Cerebellum in Sub- and Supraliminal Error Correction during Sensorimotor Synchronization: Evidence from fMRI and TMS , 2011, Journal of Cognitive Neuroscience.

[38]  A. Rangel,et al.  Dissociating valuation and saliency signals during decision-making. , 2011, Cerebral cortex.

[39]  Stephanie Ortigue,et al.  The Neural Basis of Love as a Subliminal Prime: An Event-related Functional Magnetic Resonance Imaging Study , 2007, Journal of Cognitive Neuroscience.

[40]  M. Leboyer,et al.  Conscious and subliminal conflicts in normal subjects and patients with schizophrenia: The role of the anterior cingulate , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[41]  A. Damasio.  Self comes to mind : constructing the conscious brain , 2010 .

[42]  Michael A. Olson,et al.  Implicit measures in social cognition. research: their meaning and use. , 2003, Annual review of psychology.

[43]  J. Gray,et al.  Emotional modulation of cognitive control: approach-withdrawal states double-dissociate spatial from verbal two-back task performance. , 2001, Journal of experimental psychology. General.

[44]  R. Zajonc,et al.  Affect, cognition, and awareness: affective priming with optimal and suboptimal stimulus exposures. , 1993, Journal of personality and social psychology.

[45]  T. Nickl-Jockschat,et al.  Metaanalysen in der klinischen Hirnforschung , 2009, Der Nervenarzt.

[46]  Emmanuel Dupoux,et al.  Cerebral bases of subliminal speech priming , 2010, NeuroImage.

[47]  Deborah A Yurgelun-Todd,et al.  Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces , 2004, NeuroImage.

[48]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[49]  J. Changeux,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006 Conscious, preconscious, and subliminal processing: a testable taxonomy , 2022 .

[50]  A. Craig.  Significance of the insula for the evolution of human awareness of feelings from the body. , 2011, Annals of the New York Academy of Sciences.

[51]  N. Kanwisher,et al.  The fusiform face area: a cortical region specialized for the perception of faces , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[52]  Stanislas Dehaene,et al.  Cerebral bases of subliminal and supraliminal priming during reading. , 2007, Cerebral cortex.

[53]  Reza Shaker,et al.  Cingulate cortex: a closer look at its gut-related functional topography. , 2005, American journal of physiology. Gastrointestinal and liver physiology.

[54]  Michael B. Miller,et al.  How reliable are the results from functional magnetic resonance imaging? , 2010, Annals of the New York Academy of Sciences.

[55]  Huafu Chen,et al.  Neural mechanism of unconscious perception of surprised facial expression , 2010, NeuroImage.

[56]  T. Paus.  Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[57]  M. Botvinick.  Conflict monitoring and decision making: Reconciling two perspectives on anterior cingulate function , 2007, Cognitive, affective & behavioral neuroscience.

[58]  Stephanie Ortigue,et al.  Correlation between insula activation and self-reported quality of orgasm in women , 2007, NeuroImage.

[59]  Peter Boesiger,et al.  Implicit Associative Learning Engages the Hippocampus and Interacts with Explicit Associative Learning , 2005, Neuron.

[60]  Thomas Weiss,et al.  Dynamic activation of the anterior cingulate cortex during anticipatory anxiety , 2009, NeuroImage.

[61]  S. Paradiso.  The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[62]  Harjot Sidhu,et al.  Absence of increasing cortical fMRI activity volume in response to increasing visceral stimulation in IBS patients. , 2004, American journal of physiology. Gastrointestinal and liver physiology.

[63]  A Poellinger,et al.  Brain activation responses to subliminal or supraliminal rectal stimuli and to auditory stimuli in irritable bowel syndrome , 2005, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[64]  Evian Gordon,et al.  A Direct Brainstem–amygdala–cortical Dalarmt System for Subliminal Signals of Fear , 2004 .

[65]  C M Stevenson,et al.  fMRI and MEG analysis of visceral pain in healthy volunteers , 2011, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[66]  Julie Grèzes,et al.  Look at me, I'll remember you , 2012, Human brain mapping.

[67]  Martin Wiener,et al.  The image of time: A voxel-wise meta-analysis , 2010, NeuroImage.

[68]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[69]  Jeounghoon Kim,et al.  Multiple cognitive control mechanisms associated with the nature of conflict , 2010, Neuroscience Letters.

[70]  Joy Hirsch,et al.  Self-face enhances processing of immediately preceding invisible faces , 2011, Neuropsychologia.

[71]  J B Poline,et al.  Letter Binding and Invariant Recognition of Masked Words , 2004, Psychological science.

[72]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[73]  S. Dehaene,et al.  A direct intracranial record of emotions evoked by subliminal words. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[74]  Sheng He,et al.  Dispositional fear, negative affectivity, and neuroimaging response to visually suppressed emotional faces , 2012, NeuroImage.

[75]  R. Dolan,et al.  Subliminal Instrumental Conditioning Demonstrated in the Human Brain , 2008, Neuron.

[76]  Marcin Szwed,et al.  Unconsciously deciphering handwriting: Subliminal invariance for handwritten words in the visual word form area , 2010, NeuroImage.

[77]  Joseph E LeDoux.  The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1996 .

[78]  Norihiro Sadato,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 , 2004, NeuroImage.

[79]  Cornelis G. Weststeijn,et al.  Neural representation of object location and route direction: An event-related fMRI study , 2007, Brain Research.

[80]  Rosemary A. Cowell,et al.  Components of recognition memory: Dissociable cognitive processes or just differences in representational complexity? , 2010, Hippocampus.

[81]  Stanislas Dehaene,et al.  Task-specific change of unconscious neural priming in the cerebral language network , 2007, Proceedings of the National Academy of Sciences.

[82]  Christian Büchel,et al.  Changes in connectivity profiles as a mechanism for strategic control over interfering subliminal information. , 2006, Cerebral cortex.

[83]  S. Dehaene,et al.  The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. , 2001, Cerebral cortex.

[84]  Michele T. Diaz,et al.  Unconscious Word Processing Engages a Distributed Network of Brain Regions , 2007, Journal of Cognitive Neuroscience.