Subliminal versus supraliminal stimuli activate neural responses in anterior cingulate cortex, fusiform gyrus and insula: a meta-analysis of fMRI studies

BackgroundNon-conscious neural activation may underlie various psychological functions in health and disorder. However, the neural substrates of non-conscious processing have not been entirely elucidated. Examining the differential effects of arousing stimuli that are consciously, versus unconsciously perceived will improve our knowledge of neural circuitry involved in non-conscious perception. Here we conduct preliminary analyses of neural activation in studies that have used both subliminal and supraliminal presentation of the same stimulus.MethodsWe use Activation Likelihood Estimation (ALE) to examine functional Magnetic Resonance Imaging (fMRI) studies that uniquely present the same stimuli subliminally and supraliminally to healthy participants during functional magnetic resonance imaging (fMRI). We included a total of 193 foci from 9 studies representing subliminal stimulation and 315 foci from 10 studies representing supraliminal stimulation.ResultsThe anterior cingulate cortex is significantly activated during both subliminal and supraliminal stimulus presentation. Subliminal stimuli are linked to significantly increased activation in the right fusiform gyrus and right insula. Supraliminal stimuli show significantly increased activation in the left rostral anterior cingulate.ConclusionsNon-conscious processing of arousing stimuli may involve primary visual areas and may also recruit the insula, a brain area involved in eventual interoceptive awareness. The anterior cingulate is perhaps a key brain region for the integration of conscious and non-conscious processing. These preliminary data provide candidate brain regions for further study in to the neural correlates of conscious experience.

[1]  M. Eimer,et al.  Response facilitation and inhibition in subliminal priming , 2003, Biological Psychology.

[2]  E. Soetens,et al.  Short- and Long-Term Effects of Conscious, Minimally Conscious and Unconscious Brand Logos , 2013, PloS one.

[3]  Johannes B Reitsma,et al.  Can fMRI safely replace the Wada test for preoperative assessment of language lateralisation? A meta-analysis and systematic review , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[4]  Gregor Leicht,et al.  Evidence for a close relationship between conscious effort and anterior cingulate cortex activity. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[6]  R J Seitz,et al.  Processing of subliminal facial expressions of emotion: A behavioral and fMRI study , 2013, Social neuroscience.

[7]  Leon Y. Deouell,et al.  Is there any electrophysiological evidence for subliminal error processing? , 2013, Front. Neurosci..

[8]  Rollin McCraty,et al.  Heart rate variability biofeedback, executive functioning and chronic brain injury , 2013, Brain injury.

[9]  Ezequiel Morsella,et al.  The Unconscious Mind , 2008, Perspectives on psychological science : a journal of the Association for Psychological Science.

[10]  Danilo Bzdok,et al.  The BrainMap strategy for standardization, sharing, and meta-analysis of neuroimaging data , 2011, BMC Research Notes.

[11]  G. Hall,et al.  Heightened central affective response to visceral sensations of pain and discomfort in IBS , 2010, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

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

[13]  R. Propper,et al.  Human Neuroscience Hypothesis and Theory Article Independent and Collaborative Contributions of the Cerebral Hemispheres to Emotional Processing , 2022 .

[14]  B. Baars,et al.  How conscious experience and working memory interact , 2003, Trends in Cognitive Sciences.

[15]  J. Panksepp.  Cross-Species Affective Neuroscience Decoding of the Primal Affective Experiences of Humans and Related Animals , 2011, PloS one.

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

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

[18]  A. Craig.  The sentient self , 2010, Brain Structure and Function.

[19]  Dan J Stein,et al.  Unconscious influences on decision making: Neuroimaging and neuroevolutionary perspectives , 2014, Behavioral and Brain Sciences.

[20]  W. Cannon.  The James-Lange theory of emotions: a critical examination and an alternative theory. By Walter B. Cannon, 1927. , 1927, American Journal of Psychology.

[21]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[22]  Jennifer A. Silvers,et al.  Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion , 2012, Annals of the New York Academy of Sciences.

[23]  Bruno G. Breitmeyer,et al.  Unconscious, stimulus-dependent priming and conscious, percept-dependent priming with chromatic stimuli , 2007, Perception & psychophysics.

[24]  T. Hendler,et al.  Emotional brain rhythms and their impairment in post‐traumatic patients , 2013, Human brain mapping.

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

[26]  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.

[27]  Vinod Menon,et al.  Where and When the Anterior Cingulate Cortex Modulates Attentional Response: Combined fMRI and ERP Evidence , 2006, Journal of Cognitive Neuroscience.

[28]  C. Degueldre,et al.  Here I am: The cortical correlates of visual self-recognition , 2007, Brain Research.

[29]  H. Critchley,et al.  An Interoceptive Predictive Coding Model of Conscious Presence , 2011, Front. Psychology.

[30]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[31]  Khek Yu Ho,et al.  Cortical effects of anticipation and endogenous modulation of visceral pain assessed by functional brain MRI in irritable bowel syndrome patients and healthy controls , 2006, Pain.

[32]  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.

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

[34]  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.

[35]  B. Kushner.  Descartes' error. , 1998, Journal of AAPOS : the official publication of the American Association for Pediatric Ophthalmology and Strabismus.

[36]  K. D'ostilio,et al.  Dissociation between unconscious motor response facilitation and conflict in medial frontal areas , 2012, The European journal of neuroscience.

[37]  Alfonso Caramazza,et al.  Unconscious priming instructions modulate activity in default and executive networks of the human brain. , 2012, Cerebral cortex.

[38]  Michael Erb,et al.  Non-verbal emotion communication training induces specific changes in brain function and structure , 2013, Front. Hum. Neurosci..

[39]  H. Critchley.  Neural mechanisms of autonomic, affective, and cognitive integration , 2005, The Journal of comparative neurology.

[40]  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.

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

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

[43]  Stanislas Dehaene,et al.  Distinct Brain Mechanisms for Conscious versus Subliminal Error Detection , 2022 .

[44]  Karl J. Friston,et al.  Behavioral/systems/cognitive Effective Connectivity during Processing of Facial Affect: Evidence for Multiple Parallel Pathways , 2022 .

[45]  Helgi B. Schiöth,et al.  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 , 2012, NeuroImage.

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

[47]  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.

[48]  Omri Gillath,et al.  Neural correlates of exposure to subliminal and supraliminal sexual cues. , 2012, Social cognitive and affective neuroscience.

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

[51]  Edward T. Bullmore,et al.  Differential neural responses to overt and covert presentations of facial expressions of fear and disgust , 2000, NeuroImage.

[52]  S. Slipp.  Subliminal stimulation research and its implications for psychoanalytic theory and treatment. , 2000, The Journal of the American Academy of Psychoanalysis.