REVIEW URRENT C OPINION
Visual consciousness explained by its impairments Lionel Naccache a,b
Purpose of review The scientific study of the visual consciousness has been marked by significant recent achievements, resulting from an interaction between the exploration of cognition in both brain-damaged patients and healthy individuals. Several neuropsychological syndromes contain marked dissociations which permit the identification of principles related to the neurophysiology of consciousness. The generality of these principles can then be evaluated in healthy individuals using a combination of experimental psychology paradigms, and functional brain-imaging tools. Recent findings In this article, I review major findings originating from the exploration of neuropsychological syndromes such as ‘blindsight’, visual form agnosia, optic ataxia, and neglect, and explain how they can be accounted for by a ‘global workspace’ model. Summary These results constitute important constraints for neural theories of consciousness, and they are crucial to help clinicians handle patients affected with complex neurovisual disorders. Keywords consciousness, global workspace model, unconscious perception, vision
INTRODUCTION
CONSCIOUS REPORTABILITY
Scientific investigation of consciousness has recently stimulated experimental research in healthy humans, in neurological and psychiatric patients, and in some animal models. Although this major ongoing effort does not yet provide us with a detailed and explicit neural theory of this remarkable mental faculty, we already have access to a vast collection of results acting as a set of constraints on what should be a scientific model of consciousness. There are many ways to summarize and present this set of ‘consciousness principles.’ One may either use a chronological or a domain-specific strategy. Here, I deliberately adopt a narrative approach driven by a neurological perspective, and update a previous review study [1]. This approach allows an emphasis of the crucial role played by the observation of brain-lesioned patients affected by neuropsychological syndromes. I argue that, as in other fields of cognitive neuroscience, clinical neuropsychology often offers profound insights leading to the discovery of neural principles of the physiology of consciousness [2]. Most importantly, many of these principles also prove to be relevant and to generalize to the cognition of healthy individuals.
Following the psychologist Larry Weiskrantz [3] our criterion to establish individual’s conscious perception of a stimulus will be the ‘reportability’ criteria: the ability to report explicitly to oneself or to somebody else the object of our perception: ‘I see the word consciousness printed in black on this page.’ This criterion is fully operational, and can be easily confronted to other sources of information (external reality, functional brain-imaging data), paving the way to an objective evaluation of subjective data, a scientific programme called ‘heterophenomenology’ by Daniel Dennett. How then may we use it to specify a scientific programme to investigate systematically the neural basis of visual consciousness? By first recalling that when we report a INSERM, Institut du Cerveau et de la Moelle Epinie`re and bUniversite´ Pierre et Marie Curie, Faculte´ de Me´decine Pitie´-Salpeˆtrie`re, Paris, France
Correspondence to Lionel Naccache, MD, PhD, Departments of Neurology and of Clinical Neurophysiology, Assistance Publique–Hoˆpitaux de Paris, Groupe hospitalier Pitie´-Salpeˆtrie`re Charles Foix, Paris, France. Tel: +33 1 57274314; e-mail: [email protected] Curr Opin Neurol 2015, 28:45–50 DOI:10.1097/WCO.0000000000000158
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Neuro-ophthalmology and neuro-otology
KEY POINTS Dissociations between impaired subjective reports and preserved brain processing of visual stimuli observed in neurological patients are of prime importance to theories of consciousness. Most theoretical principles stemming from the exploration of visual consciousness disorders can be generalized to the normal brain. The ‘global workspace’ model of conscious access can take into account most impairments of visual consciousness observed in neurological patients.
being conscious of seeing an object, strictly speaking we are not conscious of this object belonging to external reality, rather we are conscious of some of the visual representations elaborated in our visual brain areas and participating to the flow of our visual phenomenal consciousness. This statement foreshadows the two fundamental stages in the search of the ‘neural correlates of visual consciousness’ [4]: make a detailed inventory of the multiple representations of the visual world elaborated by different visual brain areas; and identify among these different forms of visual coding which participate in visual phenomenal consciousness, and in these cases, specify the precise conditions governing the contribution of these representations to the flow of phenomenal consciousness.
BLINDSIGHT: HIGHLIGHTING THE ROLE OF VISUAL CORTEX Some patients affected by visual scotoma secondary to primary visual cortex lesions display striking dissociations when presented with visual stimuli at the location of their scotoma. While claiming to have no conscious perception of these stimuli, they perform better than chance on forced-choice visual and visuomotor tasks such as stimulus discrimination, stimulus detection, or orientation to stimulus spatial source by visual saccades. This phenomenon, discovered in the early 1970s [5], has been coined ‘blindsight’ by Weiskrantz. Compelling evidence supports the idea that such unconscious perceptual processes are subserved by the activity of subcortical visual pathways including the superior colliculus and by-passing primary visual cortex [6]. De Gelder et al. [7] and Weiskrantz enlarged the range of unconscious perceptual processes accessible to blindsight patients by showing that patient G.Y., whose fame is comparable to that of patient H.M. in the field of medial temporal lobe amnesia, was able to discriminate better than 46
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chance emotional facial expressions on forcedchoice tasks. Taking advantage of this behavioral result, the authors used functional MRI (fMRI) to demonstrate that this affective blindsight performance correlated with activity in an extrageniculostriate colliculo-thalamo-amygdala pathway independently of both the striate cortex and fusiform face area located in the ventral pathway [8]. In fact, this unconscious visual process discovered in blindsight individuals is also active in healthy humans free of any visual cortex lesions. One way to observe it consists of using paradigms of masked or ‘subliminal’ visual stimulation in which a stimulus is briefly flashed foveally for tens of milliseconds, then immediately followed by a second stimulus, suppressing conscious perception of the former. Whalen et al. [9] used such a paradigm to mask a first fearful or neutral face by a second neutral face presented for a longer duration. Although individuals did not consciously perceive the first masked face, fMRI revealed an increase of neural activity in the amygdala on masked fearful face trials as compared with masked neutral face trials [9]. This interesting result has been replicated and enriched by a set of elegant studies conducted by Morris et al. [10,11]. The blindsight model underlines the importance of the neocortex in conscious visual processing by revealing that a subcortical pathway is able to process visual information in the absence of phenomenal consciousness. Nevertheless, should we generalize the importance shown here for the primary visual cortex – the integrity of which seems to be a prerequisite for visual consciousness – to the whole visual cortex?
VISUAL FORM AGNOSIA, OPTIC ATAXIA AND VISUAL HALLUCINATIONS: THE KEY ROLE OF THE VENTRAL PATHWAY As a result of the seminal work of Ungerleider and Mishkin [12], visual cortex anatomy is considered to be composed of two parallel and interconnected pathways both supplied by primary visual cortex area V1: the occipitotemporal or ‘ventral’ pathway and the occipitoparietal or ‘dorsal’ pathway. The dorsal pathway mainly subserves visuomotor transformations [13], whereas ventral pathway neurons represent information from low-level features to more and more abstract stages of identity processing, thus subserving object identification. This ‘what pathway’ is organized according to a posterior–anterior gradient of abstraction, the most anterior neurons located in inferotemporal cortex coding for object-based representations free from physical parameters such as retinal position, object size or orientation. Goodale et al. [14] reported a Volume 28 Number 1 February 2015
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Visual consciousness explained by its impairments Naccache
puzzling dissociation in patient D.F. suffering from severe visual form agnosia due to carbon monoxide poisoning. This patient not only had great difficulties in recognizing and identifying common objects, but she was also unable to discriminate even simple geometric forms and line orientations. Anatomically, bilateral ventral visual pathways were extensively lesioned, whereas primary visual cortices and dorsal visual pathways were spared. Goodale and Milner presented this patient with a custom ‘mailbox’, the slot of which could be rotated in the vertical plane. When asked to report slot orientation verbally or manually, patient D.F. performed at chance level, thus, confirming her persistent visual agnosia. However, when asked to post a letter into this slot she unexpectedly performed almost perfectly, although being unable to report slot orientation consciously. This spectacular observation demonstrates how spared dorsal pathway involved in visuomotor transformations was still processing visual information but without contributing to patient D.F.’s phenomenal conscious content. This case suggests that some representations elaborated in this ‘how pathway’ are operating unconsciously while ventral pathway activity subserves our phenomenal visual consciousness. Since this influential review, many studies have tested this hypothesis in healthy individuals using visual illusions. Aglioti et al. [15] engaged individuals in a Titchener–Ebbinghaus circles illusion task in which a given circle surrounded by larger circles appears smaller than the very same circle surrounded by smaller circles. Although individuals consciously reported this cognitively impenetrable illusion, when asked to grip the central circle, online measures of their thumb-index distance showed that their visuomotor response was free of the perceptual illusion and was adapted to the objective size of the circle (for a review see [16]). An inverse dissociation supporting the same general principle was recently reported by Pisella et al. [17] who demonstrated the existence of an unconscious ‘automatic pilot’ located in the dorsal pathway. Their patient I.G. presented important stroke lesions affecting both dorsal pathways, whereas sparing primary visual cortices and ventral pathways. They designed a subtle task manipulating online motor corrections of pointing movements on a tactile screen on which visual targets appeared and could unexpectedly jump from one position to another. Whereas normal individuals were capable of extremely fast and automatic visuomotor corrections in this task, patient I.G. could only rely on very slow strategic and conscious corrections. Crucially, when tested in a more complex condition in which individuals had to inhibit an initiated pointing
correction on some trials, patient I.G. committed far less errors than controls who were unable to inhibit very fast motor corrections and who reported being astonished by their own uncontrollable behavior. Taken together, these results are currently interpreted as dissociations between visuomotor processes subserved by the activity of the dorsal visual pathway, the computations of which do not always participate to our phenomenal consciousness, and other visual processes relying on ventral pathway activity that supplies our conscious perception. The strong version of this theoretical position is defended in particular by authors such as Goodale and Milner. The latter claims for instance that ‘we have two (largely) separate visual systems. One of them is dedicated to the rapid and accurate guidance of our movements. . ., and yet it lies outside the realm of our conscious visual awareness. The other seems to provide our perceptual phenomenology’ [18].
UNILATERAL SPATIAL NEGLECT: THE NECESSITY OF ATTENTIONAL ALLOCATION The recent proposal of a cerebral substrate of visual consciousness through the distinction drawn between dorsal (‘unconscious’) and ventral (‘conscious’) pathways still contains an anatomical partition between some sectors of the visual system that would supply the flow of our phenomenal consciousness, and other sectors that would process information out of our conscious awareness. However, are we necessarily conscious of all visual information represented in the ventral pathway? A key answer to this question comes from unilateral spatial neglect (USN), a very frequent neuropsychological syndrome clinically characterized by the inability to consciously perceive or respond to stimuli presented to the side contralateral to the site of lesion, despite the absence of significant sensory or motor deficits. USN syndrome is usually observed with lesions affecting the spatial attentional network – most often right parietal and/or superior temporal gyrus [19] cortices or frontoparietal white matter pathways [20], but also right thalamic or right frontal lesions – sparing primary visual cortex and the whole ventral visual pathway. Recent behavioral and functional brain-imaging studies have reliably shown that this spared visual ventral pathway still represents the neglected visual information at multiple levels of processing culminating in highly abstract forms of coding [21]. Rees et al. [22] have shown that an extinguished visual stimulus still activates corresponding retinotopic
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Neuro-ophthalmology and neuro-otology
regions of primary visual cortex and several extrastriate ventral pathway areas. In the same vein, we showed that a neglected number could be processed up to the stage of semantic coding [23]. These results demonstrate that ventral pathway activation constitutes a necessary but not sufficient condition to perceive consciously visual stimuli. The additional mechanism, defective in USN patients and mandatory to conscious perception, seems to be the top-down attentional amplification supplied by the activity of the spatial attention network [24]. We have been able to generalize this principle demonstrated by USN patients to healthy individuals, by investigating with fMRI and ERPs neural correlates of unconsciously perceived words using a visual masking procedure [25] and a repetition priming paradigm [26]. Surprisingly, a recent study showed that during transition from alertness to drowsiness, a somehow similar trend to neglect left-sided stimuli can be observed in normal controls [27]. This finding may well open new perspectives to explore more easily the mechanisms at work during neglect.
A THEORETICAL SKETCH OF CONSCIOUSNESS The observations reported above can be accounted for within the ‘global neuronal workspace’ theoretical framework developed by Dehaene et al. [28–31]. This model, in part inspired from Bernard Baars’ [32] theory, proposes that at any given time many modular cerebral networks are active in parallel and process information in an unconscious manner. Information becomes conscious, however, if the corresponding neural population is mobilized by top-down attentional amplification into a self-sustained brain-scale state of coherent activity that involves many neurons distributed throughout the brain. The long-distance connectivity of these ’workspace neurons’ can, when they are active for a minimal duration, make the information available to a variety of processes. We postulate that this global availability of information through the workspace is what we subjectively experience as a conscious state, open to introspection [33]. Neurophysiological, anatomical, and brain-imaging data strongly argue for a major role of prefrontal cortex, anterior cingulate, and the areas that connect to them, in creating the postulated brain-scale workspace. We could confirm empirically some major predictions of the global workspace model, and precise key aspects of the brain activation patterns, and oscillatory processes at work during conscious access to a visual stimulus in epileptic patients with intracranial electrodes for epilepsy presurgical 48
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mapping [34]. Whereas nonconscious processing of masked stimuli correlated with early, transient, and localized patterns of cortical activity, consciously accessed stimuli correlated with a late (corresponding to the traditional P3 scalp electro-encephalographic (EEG) pattern), sustained patterns showing long-range functional connectivity. Interestingly, we recently found the same general signature of conscious access in the auditory modality [35]. A recent fMRI study confirmed the importance of long-range coherent activity in conscious access by showing that changes in functional connectivity between low-level visual and high-level cortical areas reflect perceived stimulus visibility [36 ]. Note, however, that it remains highly difficult to demonstrate that any proposed neural signature of conscious access is not a mere correlate occurring before or after conscious access (‘upstream’ and ‘downstream’ neural correlates of consciousness) [37 ,38 ]). For instance, Pitts et al. [39] recently argued that conscious access was not systematically associated with the P3 component. However, in this interesting work, authors may have missed a delay in P3 because of a psychological refractory period effect, the presence of which is plausible in the experimental paradigm they used [40,41]. In the same vein, a recent study explored magnetoencephalographic correlates of subjective reports of stimulus visibility. Whereas early responses (100 ms) did not correlate with conscious access, late responses (290 ms) correlated moderately with it, and an intermediate response (240 ms) showed a strong correlation with conscious visibility [42]. In many different situations, strategical processing seems to be associated with conscious processing. For instance, we recently showed in a patient with a posterior split-brain lesion exposed to a task requiring to combine information originating from both hemifields that consciously perceived visual stimuli could be mobilized through the preserved anterior part of the corpus callosum [43]. Concerning the role of attentional amplification of nonconscious representation in order to access consciousness, Sergent et al. [44 ] showed very elegantly that such an amplification could even occur after the disappearance of a visual stimulus. Within this theoretical framework, the different unconscious visual processes reviewed in this article can be distinguished and explained. The activity of subcortical visual processors such as the superior colliculus, which do not possess the reciprocal connections to this global neuronal workspace that are postulated to be necessary for top-down amplification, cannot access or contribute to our conscious content, as revealed by blindsight. Moreover, the activity of other visual processors anatomically &
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Visual consciousness explained by its impairments Naccache
connected to this global workspace by reciprocal connections can still escape the content of consciousness because of top-down attentional failure. This ‘attentional failure’ may result from a direct lesion of the attentional network (such as in USN), from stringent conditions of visual presentation (such as in visual masking), or even from the evanescence of some cortical visual representations too brief to allow top-down amplification processes (such as the parietal ‘automatic pilot’ revealed by optic ataxia patients).
CONCLUSION In the present review I tried to describe how the observation of neurological patients has played a major role in the discovery of several important principles related to the neural bases of visual consciousness. However, this description is not written as a record of a heroic past era of brain sciences. On the contrary, this neuropsychology of consciousness should still provide us with exciting and unexpected observations, enabling us to tackle the most complex aspects of visual consciousness. Acknowledgements None. Financial support and sponsorship This work was supported by INSERM and FRM (‘Equipe FRM 2010’ grant). Conflicts of interest There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Naccache L. Visual consciousness: an updated neurological tour. In: Laureys S, Tononi G, editors. The neurology of consciousness. London: Academic Press; 2008. pp. 271–281. 2. Ramachandran V, Blakeslee S. Phantoms in the brain: probing the mysteries of the human mind. New York: William Morrow, Company; 1998. 3. Weiskrantz L. Consciousness lost and found: a neuropsychological exploration. New York: Oxford University Press; 1997. 4. Frith C, Perry R, Lumer E. The neural correlates of conscious experience: an experimental framework. Trends Cogn Sci 1999; 3:105–114. 5. Poppel E, Held R, Frost D. Residual visual function after brain wounds involving the central visual pathways in man. Nature 1973; 243:295– 296. 6. Cowey A, Stoerig P. The neurobiology of blindsight. Trends Neurosci 1991; 14:140–145. 7. de Gelder B, Vroomen J, Pourtois G, Weiskrantz L. Nonconscious recognition of affect in the absence of striate cortex. Neuroreport 1999; 10:3759– 3763. 8. Morris JS, DeGelder B, Weiskrantz L, Dolan RJ. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 2001; 124 (Pt 6):1241–1252.
9. Whalen PJ, Rauch SL, Etcoff NL, et al. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 1998; 18:411–418. 10. Morris JS, Ohman A, Dolan RJ. A subcortical pathway to the right amygdala mediating ‘unseen’ fear. Proc Natl Acad Sci USA 1999; 96:1680– 1685. ¨ hman A, Dolan RJ. Conscious and unconscious emotional 11. Morris JS, O learning in the human amygdala. Nature 1998; 393:467–470. 12. Ungerleider LG, Mishkin M. Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJ, editors. Analysis of visual behavior. Cambridge: MIT Press; 1982. pp. 549–586. 13. Andersen RA. Multimodal integration for the representation of space in the posterior parietal cortex. Philos Trans R Soc Lond B Biol Sci 1997; 352:1421–1428. 14. Goodale MA, Milner AD, Jakobson LS, Carey DP. A neurological dissociation between perceiving objects and grasping them. Nature 1991; 349:154– 156. 15. Aglioti S, DeSouza JF, Goodale MA. Size-contrast illusions deceive the eye but not the hand. Curr Biol 1995; 5:679–685. 16. Kwok RM, Braddick OJ. When does the Titchener Circles illusion exert an effect on grasping?. Two- and three-dimensional targets. Neuropsychologia 2003; 41:932–940. 17. Pisella L, Gre´a H, Tilikete C, et al. An ’automatic pilot’ for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia. Nat Neurosci 2000; 3:729–736. 18. Milner A. Streams and consciousness: visual consciousness and the brain. Trends Cogn Sci 1998; 2:25–30. 19. Karnath HO, Ferber S, Himmelbach M. Spatial awareness is a function of the temporal not the posterior parietal lobe. Nature 2001; 411:950– 953. 20. Thiebaut de Schotten M, Urbanski M, Duffau H, et al. Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 2005; 309:2226–2228. 21. Driver J, Vuilleumier P. Perceptual awareness and its loss in unilateral neglect and extinction. Cognition 2001; 79:39–88. 22. Rees G, Wojciulik E, Clarke K, et al. Unconscious activation of visual cortex in the damaged right hemisphere of a parietal patient with extinction. Brain 2000; 123 (Pt 8):1624–1633. 23. Sackur J, Naccache L, Pradat-Diehl P, et al. Semantic processing of neglected numbers. Cortex 2008; 44:673–682. 24. Mesulam MM. A cortical network for directed attention and unilateral neglect. Ann Neurol 1981; 10:309–315. 25. Dehaene S, Naccache L, Cohen L, et al. Cerebral mechanisms of word masking and unconscious repetition priming. Nat Neurosci 2001; 4:752– 758. 26. 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. 27. Bareham CA, Manly T, Pustovaya OV, et al. Losing the left side of the world: rightward shift in human spatial attention with sleep onset. Sci Rep 2014; 4:5092. 28. Dehaene S, Changeux JP, Naccache L, et al. Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends Cogn Sci 2006; 10:204– 211. 29. Dehaene S, Naccache L. Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework. Cognition 2001; 79:1– 37. 30. Dehaene S, Changeux JP. Experimental and theoretical approaches to conscious processing. Neuron 2011; 70:200–227. 31. Dehaene S, Changeux JP, Naccache L. The global neuronal workspace model of conscious access: from neuronal architectures to clinical applications in characterizing consciousness: from cognition to the clinic. In: Dehaene S, Christen Y, editors. Characterizing consciousness: from cognition to the clinic?. Springer: Berlin, Heidelberg; 2011. pp. 55–84. 32. Baars BJ. A cognitive theory of consciousness. Cambridge, Mass: Cambridge University Press; 1989. 33. Reyes G, Sackur J. Introspection during visual search. Conscious. Cogn 2014; 29C:212–229. 34. Gaillard R, Dehaene S, Adam C, et al. Converging intracranial markers of conscious access. PLoS Biol 2009; 7:e61. 35. El Karoui I, King JR, Sitt J, et al. Event-related potential, time-frequency, and functional connectivity facets of local and global auditory novelty processing: an intracranial study in humans. Cerebral Cortex 2014. [Epub ahead of print] 36. Imamoglu F, Heinzle J, Imfeld A, Haynes JD. Activity in high-level brain regions & reflects visibility of low-level stimuli. NeuroImage 2014; 102P2:688– 694. This study confirms the importance of high-level visual regions in conscious access to low-level stimuli, as predicted by several models including the ’global workspace.’ 37. Aru J, Bachmann T, Singer W, Melloni L. Distilling the neural correlates of & consciousness. Neurosci Biobehav Rev 2012; 36:737–746. These two reviews expose the difficulty of isolating neural signatures of consciousness from neural correlates of consciousness.
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Neuro-ophthalmology and neuro-otology 38. Sergent C, Naccache L. Imaging neural signatures of consciousness: ’what’, ’when’, ’where’ and ’how’ does it work? Archives italiennes de biologie 2012; 150:91–106. This article, contemporary to Aru et al. 2012 study, proposes a useful distinction between neural events occurring ’upstream’ (before) and ’downstream’ (after) conscious access. These two reviews expose the difficulty of isolating neural signatures of consciousness from neural correlates of consciousness. 39. Pitts MA, Padwal J, Fennelly D, et al. Gamma band activity and the P3 reflect postperceptual processes, not visual awareness. NeuroImage 2014; 101: 337–350. 40. Hesselmann G, Naccache L, Cohen L, Dehaene S. Splitting of the P3 component during dual-task processing in a patient with posterior callosal section. Cortex 2013; 49:730–747. 41. Sigman M, Dehaene S. Parsing a cognitive task: a characterization of the mind’s bottleneck. PLoS Biol 2005; 3:e37.
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42. Sekar K, Findley WM, Poeppel D, Llina´s RR. Cortical response tracking the conscious experience of threshold duration visual stimuli indicates visual perception is all or none. Proc Natl Acad Sci USA 2013; 110:5642– 5647. 43. Naccache L, Sportiche S, Strauss M, et al. Imaging ’top-down’ mobilization of visual information: a case study in a posterior split-brain patient. Neuropsychologia 2014; 53:94–103. 44. Sergent C, Wyart V, Babo-Rebelo M, et al. Cueing attention after the stimulus is gone can retrospectively trigger conscious perception. Curr Biol 2013; 23:150–155. This original study demonstrates that orienting of spatial attention can increase conscious access to stimuli presented at visibility threshold even after the disappearance of the stimuli.
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Volume 28 Number 1 February 2015
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Visual consciousness explained by its impairments Lionel Naccache a,b
Purpose of review The scientific study of the visual consciousness has been marked by significant recent achievements, resulting from an interaction between the exploration of cognition in both brain-damaged patients and healthy individuals. Several neuropsychological syndromes contain marked dissociations which permit the identification of principles related to the neurophysiology of consciousness. The generality of these principles can then be evaluated in healthy individuals using a combination of experimental psychology paradigms, and functional brain-imaging tools. Recent findings In this article, I review major findings originating from the exploration of neuropsychological syndromes such as ‘blindsight’, visual form agnosia, optic ataxia, and neglect, and explain how they can be accounted for by a ‘global workspace’ model. Summary These results constitute important constraints for neural theories of consciousness, and they are crucial to help clinicians handle patients affected with complex neurovisual disorders. Keywords consciousness, global workspace model, unconscious perception, vision
INTRODUCTION
CONSCIOUS REPORTABILITY
Scientific investigation of consciousness has recently stimulated experimental research in healthy humans, in neurological and psychiatric patients, and in some animal models. Although this major ongoing effort does not yet provide us with a detailed and explicit neural theory of this remarkable mental faculty, we already have access to a vast collection of results acting as a set of constraints on what should be a scientific model of consciousness. There are many ways to summarize and present this set of ‘consciousness principles.’ One may either use a chronological or a domain-specific strategy. Here, I deliberately adopt a narrative approach driven by a neurological perspective, and update a previous review study [1]. This approach allows an emphasis of the crucial role played by the observation of brain-lesioned patients affected by neuropsychological syndromes. I argue that, as in other fields of cognitive neuroscience, clinical neuropsychology often offers profound insights leading to the discovery of neural principles of the physiology of consciousness [2]. Most importantly, many of these principles also prove to be relevant and to generalize to the cognition of healthy individuals.
Following the psychologist Larry Weiskrantz [3] our criterion to establish individual’s conscious perception of a stimulus will be the ‘reportability’ criteria: the ability to report explicitly to oneself or to somebody else the object of our perception: ‘I see the word consciousness printed in black on this page.’ This criterion is fully operational, and can be easily confronted to other sources of information (external reality, functional brain-imaging data), paving the way to an objective evaluation of subjective data, a scientific programme called ‘heterophenomenology’ by Daniel Dennett. How then may we use it to specify a scientific programme to investigate systematically the neural basis of visual consciousness? By first recalling that when we report a INSERM, Institut du Cerveau et de la Moelle Epinie`re and bUniversite´ Pierre et Marie Curie, Faculte´ de Me´decine Pitie´-Salpeˆtrie`re, Paris, France
Correspondence to Lionel Naccache, MD, PhD, Departments of Neurology and of Clinical Neurophysiology, Assistance Publique–Hoˆpitaux de Paris, Groupe hospitalier Pitie´-Salpeˆtrie`re Charles Foix, Paris, France. Tel: +33 1 57274314; e-mail: [email protected] Curr Opin Neurol 2015, 28:45–50 DOI:10.1097/WCO.0000000000000158
1350-7540 Copyright ß 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Neuro-ophthalmology and neuro-otology
KEY POINTS Dissociations between impaired subjective reports and preserved brain processing of visual stimuli observed in neurological patients are of prime importance to theories of consciousness. Most theoretical principles stemming from the exploration of visual consciousness disorders can be generalized to the normal brain. The ‘global workspace’ model of conscious access can take into account most impairments of visual consciousness observed in neurological patients.
being conscious of seeing an object, strictly speaking we are not conscious of this object belonging to external reality, rather we are conscious of some of the visual representations elaborated in our visual brain areas and participating to the flow of our visual phenomenal consciousness. This statement foreshadows the two fundamental stages in the search of the ‘neural correlates of visual consciousness’ [4]: make a detailed inventory of the multiple representations of the visual world elaborated by different visual brain areas; and identify among these different forms of visual coding which participate in visual phenomenal consciousness, and in these cases, specify the precise conditions governing the contribution of these representations to the flow of phenomenal consciousness.
BLINDSIGHT: HIGHLIGHTING THE ROLE OF VISUAL CORTEX Some patients affected by visual scotoma secondary to primary visual cortex lesions display striking dissociations when presented with visual stimuli at the location of their scotoma. While claiming to have no conscious perception of these stimuli, they perform better than chance on forced-choice visual and visuomotor tasks such as stimulus discrimination, stimulus detection, or orientation to stimulus spatial source by visual saccades. This phenomenon, discovered in the early 1970s [5], has been coined ‘blindsight’ by Weiskrantz. Compelling evidence supports the idea that such unconscious perceptual processes are subserved by the activity of subcortical visual pathways including the superior colliculus and by-passing primary visual cortex [6]. De Gelder et al. [7] and Weiskrantz enlarged the range of unconscious perceptual processes accessible to blindsight patients by showing that patient G.Y., whose fame is comparable to that of patient H.M. in the field of medial temporal lobe amnesia, was able to discriminate better than 46
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chance emotional facial expressions on forcedchoice tasks. Taking advantage of this behavioral result, the authors used functional MRI (fMRI) to demonstrate that this affective blindsight performance correlated with activity in an extrageniculostriate colliculo-thalamo-amygdala pathway independently of both the striate cortex and fusiform face area located in the ventral pathway [8]. In fact, this unconscious visual process discovered in blindsight individuals is also active in healthy humans free of any visual cortex lesions. One way to observe it consists of using paradigms of masked or ‘subliminal’ visual stimulation in which a stimulus is briefly flashed foveally for tens of milliseconds, then immediately followed by a second stimulus, suppressing conscious perception of the former. Whalen et al. [9] used such a paradigm to mask a first fearful or neutral face by a second neutral face presented for a longer duration. Although individuals did not consciously perceive the first masked face, fMRI revealed an increase of neural activity in the amygdala on masked fearful face trials as compared with masked neutral face trials [9]. This interesting result has been replicated and enriched by a set of elegant studies conducted by Morris et al. [10,11]. The blindsight model underlines the importance of the neocortex in conscious visual processing by revealing that a subcortical pathway is able to process visual information in the absence of phenomenal consciousness. Nevertheless, should we generalize the importance shown here for the primary visual cortex – the integrity of which seems to be a prerequisite for visual consciousness – to the whole visual cortex?
VISUAL FORM AGNOSIA, OPTIC ATAXIA AND VISUAL HALLUCINATIONS: THE KEY ROLE OF THE VENTRAL PATHWAY As a result of the seminal work of Ungerleider and Mishkin [12], visual cortex anatomy is considered to be composed of two parallel and interconnected pathways both supplied by primary visual cortex area V1: the occipitotemporal or ‘ventral’ pathway and the occipitoparietal or ‘dorsal’ pathway. The dorsal pathway mainly subserves visuomotor transformations [13], whereas ventral pathway neurons represent information from low-level features to more and more abstract stages of identity processing, thus subserving object identification. This ‘what pathway’ is organized according to a posterior–anterior gradient of abstraction, the most anterior neurons located in inferotemporal cortex coding for object-based representations free from physical parameters such as retinal position, object size or orientation. Goodale et al. [14] reported a Volume 28 Number 1 February 2015
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Visual consciousness explained by its impairments Naccache
puzzling dissociation in patient D.F. suffering from severe visual form agnosia due to carbon monoxide poisoning. This patient not only had great difficulties in recognizing and identifying common objects, but she was also unable to discriminate even simple geometric forms and line orientations. Anatomically, bilateral ventral visual pathways were extensively lesioned, whereas primary visual cortices and dorsal visual pathways were spared. Goodale and Milner presented this patient with a custom ‘mailbox’, the slot of which could be rotated in the vertical plane. When asked to report slot orientation verbally or manually, patient D.F. performed at chance level, thus, confirming her persistent visual agnosia. However, when asked to post a letter into this slot she unexpectedly performed almost perfectly, although being unable to report slot orientation consciously. This spectacular observation demonstrates how spared dorsal pathway involved in visuomotor transformations was still processing visual information but without contributing to patient D.F.’s phenomenal conscious content. This case suggests that some representations elaborated in this ‘how pathway’ are operating unconsciously while ventral pathway activity subserves our phenomenal visual consciousness. Since this influential review, many studies have tested this hypothesis in healthy individuals using visual illusions. Aglioti et al. [15] engaged individuals in a Titchener–Ebbinghaus circles illusion task in which a given circle surrounded by larger circles appears smaller than the very same circle surrounded by smaller circles. Although individuals consciously reported this cognitively impenetrable illusion, when asked to grip the central circle, online measures of their thumb-index distance showed that their visuomotor response was free of the perceptual illusion and was adapted to the objective size of the circle (for a review see [16]). An inverse dissociation supporting the same general principle was recently reported by Pisella et al. [17] who demonstrated the existence of an unconscious ‘automatic pilot’ located in the dorsal pathway. Their patient I.G. presented important stroke lesions affecting both dorsal pathways, whereas sparing primary visual cortices and ventral pathways. They designed a subtle task manipulating online motor corrections of pointing movements on a tactile screen on which visual targets appeared and could unexpectedly jump from one position to another. Whereas normal individuals were capable of extremely fast and automatic visuomotor corrections in this task, patient I.G. could only rely on very slow strategic and conscious corrections. Crucially, when tested in a more complex condition in which individuals had to inhibit an initiated pointing
correction on some trials, patient I.G. committed far less errors than controls who were unable to inhibit very fast motor corrections and who reported being astonished by their own uncontrollable behavior. Taken together, these results are currently interpreted as dissociations between visuomotor processes subserved by the activity of the dorsal visual pathway, the computations of which do not always participate to our phenomenal consciousness, and other visual processes relying on ventral pathway activity that supplies our conscious perception. The strong version of this theoretical position is defended in particular by authors such as Goodale and Milner. The latter claims for instance that ‘we have two (largely) separate visual systems. One of them is dedicated to the rapid and accurate guidance of our movements. . ., and yet it lies outside the realm of our conscious visual awareness. The other seems to provide our perceptual phenomenology’ [18].
UNILATERAL SPATIAL NEGLECT: THE NECESSITY OF ATTENTIONAL ALLOCATION The recent proposal of a cerebral substrate of visual consciousness through the distinction drawn between dorsal (‘unconscious’) and ventral (‘conscious’) pathways still contains an anatomical partition between some sectors of the visual system that would supply the flow of our phenomenal consciousness, and other sectors that would process information out of our conscious awareness. However, are we necessarily conscious of all visual information represented in the ventral pathway? A key answer to this question comes from unilateral spatial neglect (USN), a very frequent neuropsychological syndrome clinically characterized by the inability to consciously perceive or respond to stimuli presented to the side contralateral to the site of lesion, despite the absence of significant sensory or motor deficits. USN syndrome is usually observed with lesions affecting the spatial attentional network – most often right parietal and/or superior temporal gyrus [19] cortices or frontoparietal white matter pathways [20], but also right thalamic or right frontal lesions – sparing primary visual cortex and the whole ventral visual pathway. Recent behavioral and functional brain-imaging studies have reliably shown that this spared visual ventral pathway still represents the neglected visual information at multiple levels of processing culminating in highly abstract forms of coding [21]. Rees et al. [22] have shown that an extinguished visual stimulus still activates corresponding retinotopic
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Neuro-ophthalmology and neuro-otology
regions of primary visual cortex and several extrastriate ventral pathway areas. In the same vein, we showed that a neglected number could be processed up to the stage of semantic coding [23]. These results demonstrate that ventral pathway activation constitutes a necessary but not sufficient condition to perceive consciously visual stimuli. The additional mechanism, defective in USN patients and mandatory to conscious perception, seems to be the top-down attentional amplification supplied by the activity of the spatial attention network [24]. We have been able to generalize this principle demonstrated by USN patients to healthy individuals, by investigating with fMRI and ERPs neural correlates of unconsciously perceived words using a visual masking procedure [25] and a repetition priming paradigm [26]. Surprisingly, a recent study showed that during transition from alertness to drowsiness, a somehow similar trend to neglect left-sided stimuli can be observed in normal controls [27]. This finding may well open new perspectives to explore more easily the mechanisms at work during neglect.
A THEORETICAL SKETCH OF CONSCIOUSNESS The observations reported above can be accounted for within the ‘global neuronal workspace’ theoretical framework developed by Dehaene et al. [28–31]. This model, in part inspired from Bernard Baars’ [32] theory, proposes that at any given time many modular cerebral networks are active in parallel and process information in an unconscious manner. Information becomes conscious, however, if the corresponding neural population is mobilized by top-down attentional amplification into a self-sustained brain-scale state of coherent activity that involves many neurons distributed throughout the brain. The long-distance connectivity of these ’workspace neurons’ can, when they are active for a minimal duration, make the information available to a variety of processes. We postulate that this global availability of information through the workspace is what we subjectively experience as a conscious state, open to introspection [33]. Neurophysiological, anatomical, and brain-imaging data strongly argue for a major role of prefrontal cortex, anterior cingulate, and the areas that connect to them, in creating the postulated brain-scale workspace. We could confirm empirically some major predictions of the global workspace model, and precise key aspects of the brain activation patterns, and oscillatory processes at work during conscious access to a visual stimulus in epileptic patients with intracranial electrodes for epilepsy presurgical 48
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mapping [34]. Whereas nonconscious processing of masked stimuli correlated with early, transient, and localized patterns of cortical activity, consciously accessed stimuli correlated with a late (corresponding to the traditional P3 scalp electro-encephalographic (EEG) pattern), sustained patterns showing long-range functional connectivity. Interestingly, we recently found the same general signature of conscious access in the auditory modality [35]. A recent fMRI study confirmed the importance of long-range coherent activity in conscious access by showing that changes in functional connectivity between low-level visual and high-level cortical areas reflect perceived stimulus visibility [36 ]. Note, however, that it remains highly difficult to demonstrate that any proposed neural signature of conscious access is not a mere correlate occurring before or after conscious access (‘upstream’ and ‘downstream’ neural correlates of consciousness) [37 ,38 ]). For instance, Pitts et al. [39] recently argued that conscious access was not systematically associated with the P3 component. However, in this interesting work, authors may have missed a delay in P3 because of a psychological refractory period effect, the presence of which is plausible in the experimental paradigm they used [40,41]. In the same vein, a recent study explored magnetoencephalographic correlates of subjective reports of stimulus visibility. Whereas early responses (100 ms) did not correlate with conscious access, late responses (290 ms) correlated moderately with it, and an intermediate response (240 ms) showed a strong correlation with conscious visibility [42]. In many different situations, strategical processing seems to be associated with conscious processing. For instance, we recently showed in a patient with a posterior split-brain lesion exposed to a task requiring to combine information originating from both hemifields that consciously perceived visual stimuli could be mobilized through the preserved anterior part of the corpus callosum [43]. Concerning the role of attentional amplification of nonconscious representation in order to access consciousness, Sergent et al. [44 ] showed very elegantly that such an amplification could even occur after the disappearance of a visual stimulus. Within this theoretical framework, the different unconscious visual processes reviewed in this article can be distinguished and explained. The activity of subcortical visual processors such as the superior colliculus, which do not possess the reciprocal connections to this global neuronal workspace that are postulated to be necessary for top-down amplification, cannot access or contribute to our conscious content, as revealed by blindsight. Moreover, the activity of other visual processors anatomically &
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Visual consciousness explained by its impairments Naccache
connected to this global workspace by reciprocal connections can still escape the content of consciousness because of top-down attentional failure. This ‘attentional failure’ may result from a direct lesion of the attentional network (such as in USN), from stringent conditions of visual presentation (such as in visual masking), or even from the evanescence of some cortical visual representations too brief to allow top-down amplification processes (such as the parietal ‘automatic pilot’ revealed by optic ataxia patients).
CONCLUSION In the present review I tried to describe how the observation of neurological patients has played a major role in the discovery of several important principles related to the neural bases of visual consciousness. However, this description is not written as a record of a heroic past era of brain sciences. On the contrary, this neuropsychology of consciousness should still provide us with exciting and unexpected observations, enabling us to tackle the most complex aspects of visual consciousness. Acknowledgements None. Financial support and sponsorship This work was supported by INSERM and FRM (‘Equipe FRM 2010’ grant). Conflicts of interest There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Naccache L. Visual consciousness: an updated neurological tour. In: Laureys S, Tononi G, editors. The neurology of consciousness. London: Academic Press; 2008. pp. 271–281. 2. Ramachandran V, Blakeslee S. Phantoms in the brain: probing the mysteries of the human mind. New York: William Morrow, Company; 1998. 3. Weiskrantz L. Consciousness lost and found: a neuropsychological exploration. New York: Oxford University Press; 1997. 4. Frith C, Perry R, Lumer E. The neural correlates of conscious experience: an experimental framework. Trends Cogn Sci 1999; 3:105–114. 5. Poppel E, Held R, Frost D. Residual visual function after brain wounds involving the central visual pathways in man. Nature 1973; 243:295– 296. 6. Cowey A, Stoerig P. The neurobiology of blindsight. Trends Neurosci 1991; 14:140–145. 7. de Gelder B, Vroomen J, Pourtois G, Weiskrantz L. Nonconscious recognition of affect in the absence of striate cortex. Neuroreport 1999; 10:3759– 3763. 8. Morris JS, DeGelder B, Weiskrantz L, Dolan RJ. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 2001; 124 (Pt 6):1241–1252.
9. Whalen PJ, Rauch SL, Etcoff NL, et al. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 1998; 18:411–418. 10. Morris JS, Ohman A, Dolan RJ. A subcortical pathway to the right amygdala mediating ‘unseen’ fear. Proc Natl Acad Sci USA 1999; 96:1680– 1685. ¨ hman A, Dolan RJ. Conscious and unconscious emotional 11. Morris JS, O learning in the human amygdala. Nature 1998; 393:467–470. 12. Ungerleider LG, Mishkin M. Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJ, editors. Analysis of visual behavior. Cambridge: MIT Press; 1982. pp. 549–586. 13. Andersen RA. Multimodal integration for the representation of space in the posterior parietal cortex. Philos Trans R Soc Lond B Biol Sci 1997; 352:1421–1428. 14. Goodale MA, Milner AD, Jakobson LS, Carey DP. A neurological dissociation between perceiving objects and grasping them. Nature 1991; 349:154– 156. 15. Aglioti S, DeSouza JF, Goodale MA. Size-contrast illusions deceive the eye but not the hand. Curr Biol 1995; 5:679–685. 16. Kwok RM, Braddick OJ. When does the Titchener Circles illusion exert an effect on grasping?. Two- and three-dimensional targets. Neuropsychologia 2003; 41:932–940. 17. Pisella L, Gre´a H, Tilikete C, et al. An ’automatic pilot’ for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia. Nat Neurosci 2000; 3:729–736. 18. Milner A. Streams and consciousness: visual consciousness and the brain. Trends Cogn Sci 1998; 2:25–30. 19. Karnath HO, Ferber S, Himmelbach M. Spatial awareness is a function of the temporal not the posterior parietal lobe. Nature 2001; 411:950– 953. 20. Thiebaut de Schotten M, Urbanski M, Duffau H, et al. Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 2005; 309:2226–2228. 21. Driver J, Vuilleumier P. Perceptual awareness and its loss in unilateral neglect and extinction. Cognition 2001; 79:39–88. 22. Rees G, Wojciulik E, Clarke K, et al. Unconscious activation of visual cortex in the damaged right hemisphere of a parietal patient with extinction. Brain 2000; 123 (Pt 8):1624–1633. 23. Sackur J, Naccache L, Pradat-Diehl P, et al. Semantic processing of neglected numbers. Cortex 2008; 44:673–682. 24. Mesulam MM. A cortical network for directed attention and unilateral neglect. Ann Neurol 1981; 10:309–315. 25. Dehaene S, Naccache L, Cohen L, et al. Cerebral mechanisms of word masking and unconscious repetition priming. Nat Neurosci 2001; 4:752– 758. 26. 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. 27. Bareham CA, Manly T, Pustovaya OV, et al. Losing the left side of the world: rightward shift in human spatial attention with sleep onset. Sci Rep 2014; 4:5092. 28. Dehaene S, Changeux JP, Naccache L, et al. Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends Cogn Sci 2006; 10:204– 211. 29. Dehaene S, Naccache L. Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework. Cognition 2001; 79:1– 37. 30. Dehaene S, Changeux JP. Experimental and theoretical approaches to conscious processing. Neuron 2011; 70:200–227. 31. Dehaene S, Changeux JP, Naccache L. The global neuronal workspace model of conscious access: from neuronal architectures to clinical applications in characterizing consciousness: from cognition to the clinic. In: Dehaene S, Christen Y, editors. Characterizing consciousness: from cognition to the clinic?. Springer: Berlin, Heidelberg; 2011. pp. 55–84. 32. Baars BJ. A cognitive theory of consciousness. Cambridge, Mass: Cambridge University Press; 1989. 33. Reyes G, Sackur J. Introspection during visual search. Conscious. Cogn 2014; 29C:212–229. 34. Gaillard R, Dehaene S, Adam C, et al. Converging intracranial markers of conscious access. PLoS Biol 2009; 7:e61. 35. El Karoui I, King JR, Sitt J, et al. Event-related potential, time-frequency, and functional connectivity facets of local and global auditory novelty processing: an intracranial study in humans. Cerebral Cortex 2014. [Epub ahead of print] 36. Imamoglu F, Heinzle J, Imfeld A, Haynes JD. Activity in high-level brain regions & reflects visibility of low-level stimuli. NeuroImage 2014; 102P2:688– 694. This study confirms the importance of high-level visual regions in conscious access to low-level stimuli, as predicted by several models including the ’global workspace.’ 37. Aru J, Bachmann T, Singer W, Melloni L. Distilling the neural correlates of & consciousness. Neurosci Biobehav Rev 2012; 36:737–746. These two reviews expose the difficulty of isolating neural signatures of consciousness from neural correlates of consciousness.
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Neuro-ophthalmology and neuro-otology 38. Sergent C, Naccache L. Imaging neural signatures of consciousness: ’what’, ’when’, ’where’ and ’how’ does it work? Archives italiennes de biologie 2012; 150:91–106. This article, contemporary to Aru et al. 2012 study, proposes a useful distinction between neural events occurring ’upstream’ (before) and ’downstream’ (after) conscious access. These two reviews expose the difficulty of isolating neural signatures of consciousness from neural correlates of consciousness. 39. Pitts MA, Padwal J, Fennelly D, et al. Gamma band activity and the P3 reflect postperceptual processes, not visual awareness. NeuroImage 2014; 101: 337–350. 40. Hesselmann G, Naccache L, Cohen L, Dehaene S. Splitting of the P3 component during dual-task processing in a patient with posterior callosal section. Cortex 2013; 49:730–747. 41. Sigman M, Dehaene S. Parsing a cognitive task: a characterization of the mind’s bottleneck. PLoS Biol 2005; 3:e37.
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42. Sekar K, Findley WM, Poeppel D, Llina´s RR. Cortical response tracking the conscious experience of threshold duration visual stimuli indicates visual perception is all or none. Proc Natl Acad Sci USA 2013; 110:5642– 5647. 43. Naccache L, Sportiche S, Strauss M, et al. Imaging ’top-down’ mobilization of visual information: a case study in a posterior split-brain patient. Neuropsychologia 2014; 53:94–103. 44. Sergent C, Wyart V, Babo-Rebelo M, et al. Cueing attention after the stimulus is gone can retrospectively trigger conscious perception. Curr Biol 2013; 23:150–155. This original study demonstrates that orienting of spatial attention can increase conscious access to stimuli presented at visibility threshold even after the disappearance of the stimuli.
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