From affective blindsight to emotional consciousness

Following destruction or denervation of the primary visual cortex (V1) cortical blindness ensues. Affective blindsight refers to the uncanny ability of such patients to respond correctly, or above chance level, to visual emotional expressions presented to their blind fields. Fifteen years after its original discovery, affective blindsight still fascinates neuroscientists and philosophers alike, as it offers a unique window on the vestigial properties of our visual system that, though present in the intact brain, tend to be unnoticed or even actively inhibited by conscious processes. Here we review available studies on affective blindsight with the intent to clarify its functional properties, neural bases and theoretical implications. Evidence converges on the role of subcortical structures of old evolutionary origin such as the superior colliculus, the pulvinar and the amygdala in mediating affective blindsight and nonconscious perception of emotions. We conclude that approaching consciousness, and its absence, from the vantage point of emotion processing may uncover important relations between the two phenomena, as consciousness may have evolved as an evolutionary specialization to interact with others and become aware of their social and emotional expressions.

[1]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[2]  C. Marzi,et al.  Blindsight is sensitive to stimulus numerosity and configuration: evidence from the redundant signal effect , 2015, Experimental Brain Research.

[3]  L. Pessoa To what extent are emotional visual stimuli processed without attention and awareness? , 2005, Current Opinion in Neurobiology.

[4]  Changjun Shi,et al.  Visual Pathways Involved in Fear Conditioning Measured with Fear-Potentiated Startle: Behavioral and Anatomic Studies , 2001, The Journal of Neuroscience.

[5]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[6]  L Weiskrantz,et al.  Pattern of neuronal activity associated with conscious and unconscious processing of visual signals. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Fox On Unconscious Emotions , 1973 .

[8]  B. Wandell,et al.  Topographic Organization of Human Visual Areas in the Absence of Input from Primary Cortex , 1999, The Journal of Neuroscience.

[9]  Daniel Tranel,et al.  Preferring one taste over another without recognizing either , 2005, Nature Neuroscience.

[10]  A. Cowey,et al.  Is blindsight like normal, near-threshold vision? , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[11]  M. Davis,et al.  Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  D. Chalmers Consciousness and Cognition , 1990 .

[13]  A. Anderson,et al.  Neural Correlates of the Automatic Processing of Threat Facial Signals , 2022 .

[14]  C. A. Marzi,et al.  Spatial summation across the vertical meridian in hemianopics: A test of blindsight , 1986, Neuropsychologia.

[15]  Oliver G. B. Garrod,et al.  Dynamic Facial Expressions of Emotion Transmit an Evolving Hierarchy of Signals over Time , 2014, Current Biology.

[16]  Nicholas Humphrey,et al.  Consciousness Regained: Chapters in the Development of Mind , 1983 .

[17]  Gilles Pourtois,et al.  Affective blindsight: are we blindly led by emotions? Response to Heywood and Kentridge (2000) , 2000, Trends in Cognitive Sciences.

[18]  Raymond J. Dolan,et al.  Subcortical amygdala pathways enable rapid face processing , 2014, NeuroImage.

[19]  Robert Ward,et al.  Response to Visual Threat Following Damage to the Pulvinar , 2005, Current Biology.

[20]  D. Mitchell,et al.  Conscious Perception of Emotional Stimuli , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[21]  H. Pape,et al.  Direct synaptic connections of axons from superior colliculus with identified thalamo‐amygdaloid projection neurons in the rat: Possible substrates of a subcortical visual pathway to the amygdala , 1999, The Journal of comparative neurology.

[22]  A. Cantagallo,et al.  Speeded manual responses to unseen visual stimuli in hemianopic patients: What kind of blindsight? , 2015, Consciousness and Cognition.

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

[24]  L Weiskrantz,et al.  Unseen stimuli modulate conscious visual experience: evidence from inter-hemispheric summation , 2001, Neuroreport.

[25]  Robert Ward,et al.  Emotion recognition following human pulvinar damage , 2007, Neuropsychologia.

[26]  R. Dolan,et al.  Distinct spatial frequency sensitivities for processing faces and emotional expressions , 2003, Nature Neuroscience.

[27]  B. Gelder Towards the neurobiology of emotional body language , 2006, Nature Reviews Neuroscience.

[28]  Brian Zingg,et al.  Sensory Cortical Control of a Visually Induced Arrest Behavior via Corticotectal Projections , 2015, Neuron.

[29]  Swann Pichon,et al.  Cortico-subcortical visual, somatosensory, and motor activations for perceiving dynamic whole-body emotional expressions with and without striate cortex (V1) , 2011, Proceedings of the National Academy of Sciences.

[30]  Alan Cowey,et al.  The 30th Sir Frederick Bartlett Lecture: Fact, Artefact, and Myth about Blindsight , 2004, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[31]  R. Dolan,et al.  Unconscious fear influences emotional awareness of faces and voices. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Adam P. Morris,et al.  Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression , 2004, The Journal of Neuroscience.

[33]  A. Damasio The Feeling of What Happens: Body and Emotion in the Making of Consciousness , 1999 .

[34]  L Weiskrantz,et al.  The Ferrier Lecture, 1989 - Outlooks for blindsight: explicit methodologies for implicit processes , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[35]  Henry Railo,et al.  Unlike in Clinical Blindsight Patients, Unconscious Processing of Chromatic Information Depends on Early Visual Cortex in Healthy Humans , 2014, Brain Stimulation.

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

[37]  V. Gazzola,et al.  Seeing fearful body language rapidly freezes the observer's motor cortex , 2015, Cortex.

[38]  R. Held,et al.  Residual Visual Function after Brain Wounds involving the Central Visual Pathways in Man , 1973, Nature.

[39]  L. Weiskrantz,et al.  Behavioral changes associated with ablation of the amygdaloid complex in monkeys. , 1956, Journal of comparative and physiological psychology.

[40]  L Weiskrantz,et al.  Early extrastriate activity without primary visual cortex in humans , 2000, Neuroscience Letters.

[41]  R. J. Dolan,et al.  Human Amygdala Responses to Fearful Eyes , 2002, NeuroImage.

[42]  Geraint Rees,et al.  Neural correlates of consciousness in humans , 2002, Nature Reviews Neuroscience.

[43]  Alain Ptito,et al.  Absence of S‐cone input in human blindsight following hemispherectomy , 2006, The European journal of neuroscience.

[44]  A. Cowey The blindsight saga , 2009, Experimental Brain Research.

[45]  Gilles Pourtois,et al.  Fear recognition in the voice is modulated by unconsciously recognized facial expressions but not by unconsciously recognized affective pictures , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[46]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[47]  Justin A. Harris,et al.  Brain-Stimulation Induced Blindsight: Unconscious Vision or Response Bias? , 2013, PloS one.

[48]  Rainer Goebel,et al.  Sustained extrastriate cortical activation without visual awareness revealed by fMRI studies of hemianopic patients , 2001, Vision Research.

[49]  Joseph E LeDoux,et al.  Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat , 1999, The Journal of comparative neurology.

[50]  L. Weiskrantz,et al.  Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. , 2001, Brain : a journal of neurology.

[51]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[52]  M. Bickford,et al.  Neuroanatomy Original Research Article , 2022 .

[53]  Béatrice de Gelder,et al.  Affective blindsight , 2007, Scholarpedia.

[54]  Christopher D. Chambers,et al.  The Timing and Neuroanatomy of Conscious Vision as Revealed by TMS-induced Blindsight , 2014, Journal of Cognitive Neuroscience.

[55]  S. Shimojo,et al.  Faces, bodies, social vision as agent vision, and social consciousness , 2010 .

[56]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.

[57]  M. Mallar Chakravarty,et al.  Blindsight Mediated by an S-Cone-independent Collicular Pathway: An fMRI Study in Hemispherectomized Subjects , 2010, Journal of Cognitive Neuroscience.

[58]  Morten Overgaard,et al.  Visual experience and blindsight: a methodological review , 2011, Experimental Brain Research.

[59]  Caterina Bertini,et al.  Unseen Fearful Faces Influence Face Encoding: Evidence from ERPs in Hemianopic Patients , 2014, Journal of Cognitive Neuroscience.

[60]  Saâd Jbabdi,et al.  Changes in connectivity after visual cortical brain damage underlie altered visual function. , 2008, Brain : a journal of neurology.

[61]  Heidi Johansen-Berg,et al.  Unconscious vision: new insights into the neuronal correlate of blindsight using diffusion tractography. , 2006, Brain : a journal of neurology.

[62]  Marco Tamietto,et al.  Attention and awareness each influence amygdala activity for dynamic bodily expressions—a short review , 2012, Front. Integr. Neurosci..

[63]  Marco Tamietto,et al.  Visual imagery influences brain responses to visual stimulation in bilateral cortical blindness , 2015, Cortex.

[64]  L Weiskrantz,et al.  Visual capacity in the hemianopic field following a restricted occipital ablation. , 1974, Brain : a journal of neurology.

[65]  Hisao Nishijo,et al.  The monkey pulvinar neurons differentially respond to emotional expressions of human faces , 2010, Behavioural Brain Research.

[66]  U. Dimberg,et al.  Unconscious Facial Reactions to Emotional Facial Expressions , 2000, Psychological science.

[67]  Barbara Pfeffer Out Of Mind Varieties Of Unconscious Processes , 2016 .

[68]  Giuliano Geminiani,et al.  Effects of emotional face cueing on line bisection in neglect: A single case study , 2005, Neurocase.

[69]  L Weiskrantz,et al.  Non-conscious recognition of affect in the absence of striate cortex. , 1999, Neuroreport.

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

[71]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[72]  Robert D. Rafal,et al.  Connectivity between the superior colliculus and the amygdala in humans and macaque monkeys: virtual dissection with probabilistic DTI tractography , 2015, Journal of neurophysiology.

[73]  K M Gothard,et al.  Neural responses to facial expression and face identity in the monkey amygdala. , 2007, Journal of neurophysiology.

[74]  R. Adolphs,et al.  Emotion and consciousness , 2007, Trends in Cognitive Sciences.

[75]  R. James R. Blair,et al.  Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG , 2007, NeuroImage.

[76]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[77]  A. Cowey,et al.  Abnormal functional connectivity between ipsilesional V5/MT+ and contralesional striate cortex (V1) in blindsight , 2009, Experimental Brain Research.

[78]  A. Damasio,et al.  The nature of feelings: evolutionary and neurobiological origins , 2013, Nature Reviews Neuroscience.

[79]  J. Cacioppo,et al.  Emotional Contagion , 1993 .

[80]  M. Tamietto,et al.  Neural bases of the non-conscious perception of emotional signals , 2010, Nature Reviews Neuroscience.

[81]  Leslie G. Ungerleider,et al.  Visual awareness and the detection of fearful faces. , 2005, Emotion.

[82]  U. Dimberg Facial reactions to facial expressions. , 1982, Psychophysiology.

[83]  M. Tamietto,et al.  Functional asymmetry and interhemispheric cooperation in the perception of emotions from facial expressions , 2006, Experimental Brain Research.

[84]  Harald T Schupp,et al.  Affective blindsight: intact fear conditioning to a visual cue in a cortically blind patient. , 2003, Brain : a journal of neurology.

[85]  Jac Billington,et al.  Neural processing of imminent collision in humans , 2011, Proceedings of the Royal Society B: Biological Sciences.

[86]  Asaid Khateb,et al.  Discriminating emotional faces without primary visual cortices involves the right amygdala , 2005, Nature Neuroscience.

[87]  Michael Davis,et al.  Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear- potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[88]  Michael Hogan Consciousness of brain , 2006 .

[89]  Beatrice de Gelder,et al.  Out of Mind : Varieties of Unconscious Processes , 2001 .

[90]  Asaid Khateb,et al.  Electrophysiological correlates of affective blindsight , 2009, NeuroImage.

[91]  Marco Tamietto,et al.  Emotion in the brain: of low roads, high roads and roads less travelled , 2011, Nature Reviews Neuroscience.

[92]  Terrence J. Sejnowski,et al.  Inhibition synchronizes sparsely connected cortical neurons within and between columns in realistic network models , 1996, Journal of Computational Neuroscience.

[93]  Jeffrey S. Maxwell,et al.  Human Amygdala Responsivity to Masked Fearful Eye Whites , 2004, Science.

[94]  The (Non)Automaticity of Amygdala Responses to Threat: On the Issue of Fast Signals and Slow Measures , 2011, The Journal of Neuroscience.

[95]  Falk Eippert,et al.  When seeing outweighs feeling: a role for prefrontal cortex in passive control of negative affect in blindsight , 2009 .

[96]  Michael Erb,et al.  Parietal somatosensory association cortex mediates affective blindsight , 2004, Nature Neuroscience.

[97]  Christopher J Rennie,et al.  Mode of Functional Connectivity in Amygdala Pathways Dissociates Level of Awareness for Signals of Fear , 2006, The Journal of Neuroscience.

[98]  C. Tallon-Baudry,et al.  The neural subjective frame: from bodily signals to perceptual consciousness , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[99]  B. de Gelder,et al.  Neural correlates of body and face perception following bilateral destruction of the primary visual cortices , 2014, Front. Behav. Neurosci..

[100]  Béatrice de Gelder,et al.  Collicular Vision Guides Nonconscious Behavior , 2010, Journal of Cognitive Neuroscience.

[101]  K H Ruddock,et al.  Human visual responses in the absence of the geniculo-calcarine projection. , 1980, Brain : a journal of neurology.

[102]  M. Tamietto,et al.  Body Recognition in a Patient with Bilateral Primary Visual Cortex Lesions , 2015, Biological Psychiatry.

[103]  Nouchine Hadjikhani,et al.  Non-conscious recognition of emotional body language , 2006, Neuroreport.

[104]  P. Redgrave,et al.  Segregated Anatomical Input to Sub-Regions of the Rodent Superior Colliculus Associated with Approach and Defense , 2012, Front. Neuroanat..

[105]  Rainer Goebel,et al.  Subcortical Connections to Human Amygdala and Changes following Destruction of the Visual Cortex , 2012, Current Biology.

[106]  Leanne M Williams,et al.  Mapping the time course of nonconscious and conscious perception of fear: An integration of central and peripheral measures , 2004, Human brain mapping.

[107]  E. Làdavas,et al.  I am blind, but I “see” fear , 2013, Cortex.

[108]  E. G. Jones,et al.  A projection from the medial pulvinar to the amygdala in primates , 1976, Brain Research.

[109]  Brian N. Pasley,et al.  Subcortical Discrimination of Unperceived Objects during Binocular Rivalry , 2004, Neuron.

[110]  Katiuscia Sacco,et al.  Once you feel it, you see it: Insula and sensory-motor contribution to visual awareness for fearful bodies in parietal neglect , 2015, Cortex.

[111]  M. Bar,et al.  Exploring the unconscious using faces , 2015, Trends in Cognitive Sciences.

[112]  J. Panksepp Affective consciousness: Core emotional feelings in animals and humans , 2005, Consciousness and Cognition.

[113]  S. Monsell,et al.  TMS to V1 spares discrimination of emotive relative to neutral body postures , 2013, Neuropsychologia.

[114]  Marco Tamietto,et al.  Affective blindsight in the intact brain: Neural interhemispheric summation for unseen fearful expressions , 2008, Neuropsychologia.

[115]  V. Lamme,et al.  Repression of unconscious information by conscious processing: evidence from affective blindsight induced by transcranial magnetic stimulation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[116]  Patrik Vuilleumier,et al.  Fear and stop: A role for the amygdala in motor inhibition by emotional signals , 2011, NeuroImage.

[117]  T. Holroyd,et al.  Emotional Automaticity Is a Matter of Timing , 2010, The Journal of Neuroscience.

[118]  Joseph E LeDoux The emotional brain , 1996 .

[119]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[120]  Franco Cauda,et al.  Temporal and spatial neural dynamics in the perception of basic emotions from complex scenes. , 2014, Social cognitive and affective neuroscience.

[121]  Jumpei Matsumoto,et al.  Neuronal responses to face-like and facial stimuli in the monkey superior colliculus , 2014, Front. Behav. Neurosci..

[122]  Alexis Hervais-Adelman,et al.  Amygdala Activation for Eye Contact Despite Complete Cortical Blindness , 2013, The Journal of Neuroscience.

[123]  V. Gazzola,et al.  Transcranial magnetic stimulation reveals two functionally distinct stages of motor cortex involvement during perception of emotional body language , 2014, Brain Structure and Function.

[124]  Giuliano Geminiani,et al.  Unseen facial and bodily expressions trigger fast emotional reactions , 2009, Proceedings of the National Academy of Sciences.

[125]  Katsuki Nakamura,et al.  Responses of single neurons in monkey amygdala to facial and vocal emotions. , 2007, Journal of neurophysiology.

[126]  Marta I. Garrido,et al.  Functional Evidence for a Dual Route to Amygdala , 2012, Current Biology.