Spotlight
Is primary visual cortex necessary for visual awareness? Juha Silvanto Department of Psychology, Faculty of Science and Technology, University of Westminster, 115 New Cavendish Street, W1W 6UW, London, UK Brain Research Unit, O.V. Lounasmaa Laboratory, School of Science, Aalto University, PO BOX 15100, 00076 Aalto, Finland
Influential models propose that conscious experience of extrastriate activity requires the integrity of primary visual cortex (V1). A new study challenges this view by demonstrating that when V1 is lesioned, visual qualia can be induced when transcranial magnetic stimulation (TMS) is applied over the patients’ ipsilesional hemisphere. According to hierarchical models of visual processing, only high-level extrastriate regions contribute directly to conscious experience; the role of low-level areas such as the primary visual cortex (V1) is to merely feed information forward to upper levels of the cortical hierarchy [1]. This view has been challenged by blindsight, a neuropsychological phenomenon in which lesion to V1 abolishes all visual awareness, yet extrastriate regions remain capable of processing information in an unconscious manner (see e.g., [2] for review). A key aspect of blindsight is that the loss of awareness cannot be explained by a lack of input to higher-level regions, as these continue to receive and process feedforward input via pathways bypassing V1 [3]. The theoretical implication is that extrastriate cortex requires the involvement of V1 in order for its activation to reach awareness. The ‘blindness’ of blindsight has often been explained in terms of feedback connections from extrastriate regions to V1 acting as a gatekeeper of awareness (see e.g., [4,5]). In this view, extrastriate activation needs to be fed back to V1 in order for the content of that activation to be consciously perceived. While unconscious visuo-motor transformations (as in blindsight) can be executed in an entirely feedforward processing cycle, visual awareness is critically dependent on this feedback [6]. This view has been challenged by a recent study by Mazzi et al. [7], who used transcranial magnetic stimulation (TMS) in an attempt to induce conscious visual experiences in two patients with unilateral V1 lesions. When applied over visual cortical regions of healthy volunteers, TMS can induce the perception of phosphenes (brief flashes of light), which result from the direct activation of neurons involved in visual processing. According to the feedback model [6], phosphene perception should not be possible when TMS is applied over intact regions of the damaged Corresponding author: Silvanto, J. ([email protected]). 0166-2236/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tins.2014.09.006
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hemisphere, as there is no V1 for the induced activation to feed back to; that is, the gateway into awareness is absent. Inconsistent with this view, both patients tested by Mazzi et al. could perceive phosphenes in their blind hemifields when ipsilesional parietal regions were stimulated. Furthermore, a psychophysical threshold function of phosphene perception could be obtained, which did not differ from those obtained in neurologically normal control participants. Thus, in the absence of V1, phosphenes can be perceived, with similar properties as those induced in neurologically normal observers. The theoretical implication is that V1 is not necessary for visual awareness under all circumstances. There are previous reports of patients with unilateral V1 lesions experiencing visual qualia. Hemianopic completion can occur when visual stimuli are presented across the vertical meridian such that one half of the figure falls within the blind hemifield and the other on the sighted field. Some patients are able to perceive the complete figure, including the blind field component, whereas there is no conscious experience when none of the figure intrudes the sighted field (e.g., [8]). There is also prior evidence of TMS-induced percepts in such patients. When TMS was applied over the visual motion area V5/MT+ bilaterally (i.e., both the damaged and intact hemisphere were stimulated with TMS in close temporal proximity), a blindsight subject could perceive bilateral phosphenes [9]. However, in these prior studies, the contribution of the intact hemisphere was required. This was not the case in the study of Mazzi et al., in which qualia could be induced selectively from the ipsilesional hemisphere and experienced exclusively in the blind field. This was not the first attempt to induce phosphenes in patients without V1. In a previous study, application of TMS over the motion-selective area V5/MT in the damaged hemisphere of a blindsight patient did not generate phosphenes [10]. Why the previous attempt failed while Mazzi et al succeeded is an open question. It might relate to the fact that brain lesions are heterogeneous; for example, the patient studied in [10] has lesions beyond V1, including the parietal cortex [11]. Determining the neural correlates of TMS-induced activity and phosphene perception in the absence of V1 by combining TMS with neuroimaging techniques such as EEG or fMRI might help to resolve this discrepancy. The findings of Mazzi et al demonstrate that when V1 is damaged, the affected hemisphere can still generate visual qualia. However, the fact remains that patients with V1
Spotlight lesions are phenomenally blind to visual input. For reasons that require further research, TMS in the study of Mazzi et al. was able to induce the conditions in which visual awareness can arise. What might these conditions be? One possibility is that visual awareness requires inter-areal neural synchrony, established through cortico-cortical feedback (e.g., [12,13,15]), and V1 might be indispensible in this process because it engages in recurrent activity with the majority of extrastriate visual regions [15]. Indeed, V1 is instrumental in enabling normal visual responsiveness to external input throughout the visual cortex; when it is lesioned, extrastriate responses become sluggish, and exhibit abnormally bursty spontaneous activity and high response variability [3,14]. Perhaps inter-areal synchrony cannot arise in the absence of V1, yet it can be artificially induced by TMS, because the application of a TMS pulse simultaneously depolarises a sizeable population of neurons and induces large-scale synchronous neural firing. Furthermore, one might speculate that low-level unconscious visual functions (as found in blindsight) may still be possible in the absence of inter-areal synchrony, in the form of ‘local’ neural readout from individual extrastriate regions [15]. The study of Mazzi et al. sheds new light on the functional role of V1 by demonstrating that this region cannot be the only gateway into visual awareness. However, the fact remains that its lesion abolishes the ability to consciously perceive external visual input. Even though extrastriate regions continue to process visual information in the absence of V1, qualia can be experienced in only very limited circumstances. The challenge now is to decipher those circumstances, as they may give fundamental clues
Trends in Neurosciences November 2014, Vol. 37, No. 11
about the neural processes underlying conscious visual perception. V1 and feedback connections may still be implicated [4–6,13,15]. The question is: how? References 1 Crick, F. and Koch, C. (1995) Are we aware of neural activity in primary visual cortex? Nature 375, 121–123 2 Cowey, A. (2010) The blindsight saga. Exp. Brain Res. 200, 3–24 3 Rodman, H.R. et al. (1989) Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal. J. Neurosci. 9, 2033–2050 4 Stoerig, P. and Cowey, A. (1995) Visual perception and phenomenal consciousness. Behav. Brain Res. 71, 147–156 5 Weiskrantz, L. (1997) Consciousness lost and found, Oxford University Press, (Oxford) 6 Lamme, V.A. (2003) Why visual attention and awareness are different. Trends Cogn. Sci. 7, 12–18 7 Mazzi, C. et al. (2014) Can IPS reach visual awareness without V1? Evidence from TMS in healthy subjects and hemianopic patients. Neuropsychologia 64, 134–144 8 Bender, M.B. and Kahn, R.L. (1949) After-imagery in defective fields of vision. J. Neurol. Neurosurg. Psychiatry 12, 196–204 9 Silvanto, J. et al. (2007) Making the blindsighted see. Neuropsychologia 45, 3346–3350 10 Cowey, A. and Walsh, V. (2000) Magnetically induced phosphenes in sighted, blind and blindsighted observers. Neuroreport 11, 3269–3273 11 Bridge, H. et al. (2008) Changes in connectivity after visual cortical brain damage underlie altered visual function. Brain 131, 1433–1444 12 Dehaene, S. and Changeux, J.P. (2011) Experimental and theoretical approaches to conscious processing. Neuron 70, 200–227 13 Pollen, D.A. (1999) On the neural correlates of visual perception. Cereb. Cortex 9, 4–19 14 Azzopardi, P. et al. (2003) Response latencies of neurons in visual areas MT and MST of monkeys with striate cortex lesions. Neuropsychologia 41, 1738–1756 15 Silvanto, J. (2014) Why is ‘‘blindsight’’ blind?. A new perspective on primary visual cortex, feedback and visual awareness. Conscious. Cogn. http://dx.doi.org/10.1016/j.concog.2014.08.001
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Is primary visual cortex necessary for visual awareness? Juha Silvanto Department of Psychology, Faculty of Science and Technology, University of Westminster, 115 New Cavendish Street, W1W 6UW, London, UK Brain Research Unit, O.V. Lounasmaa Laboratory, School of Science, Aalto University, PO BOX 15100, 00076 Aalto, Finland
Influential models propose that conscious experience of extrastriate activity requires the integrity of primary visual cortex (V1). A new study challenges this view by demonstrating that when V1 is lesioned, visual qualia can be induced when transcranial magnetic stimulation (TMS) is applied over the patients’ ipsilesional hemisphere. According to hierarchical models of visual processing, only high-level extrastriate regions contribute directly to conscious experience; the role of low-level areas such as the primary visual cortex (V1) is to merely feed information forward to upper levels of the cortical hierarchy [1]. This view has been challenged by blindsight, a neuropsychological phenomenon in which lesion to V1 abolishes all visual awareness, yet extrastriate regions remain capable of processing information in an unconscious manner (see e.g., [2] for review). A key aspect of blindsight is that the loss of awareness cannot be explained by a lack of input to higher-level regions, as these continue to receive and process feedforward input via pathways bypassing V1 [3]. The theoretical implication is that extrastriate cortex requires the involvement of V1 in order for its activation to reach awareness. The ‘blindness’ of blindsight has often been explained in terms of feedback connections from extrastriate regions to V1 acting as a gatekeeper of awareness (see e.g., [4,5]). In this view, extrastriate activation needs to be fed back to V1 in order for the content of that activation to be consciously perceived. While unconscious visuo-motor transformations (as in blindsight) can be executed in an entirely feedforward processing cycle, visual awareness is critically dependent on this feedback [6]. This view has been challenged by a recent study by Mazzi et al. [7], who used transcranial magnetic stimulation (TMS) in an attempt to induce conscious visual experiences in two patients with unilateral V1 lesions. When applied over visual cortical regions of healthy volunteers, TMS can induce the perception of phosphenes (brief flashes of light), which result from the direct activation of neurons involved in visual processing. According to the feedback model [6], phosphene perception should not be possible when TMS is applied over intact regions of the damaged Corresponding author: Silvanto, J. ([email protected]). 0166-2236/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tins.2014.09.006
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hemisphere, as there is no V1 for the induced activation to feed back to; that is, the gateway into awareness is absent. Inconsistent with this view, both patients tested by Mazzi et al. could perceive phosphenes in their blind hemifields when ipsilesional parietal regions were stimulated. Furthermore, a psychophysical threshold function of phosphene perception could be obtained, which did not differ from those obtained in neurologically normal control participants. Thus, in the absence of V1, phosphenes can be perceived, with similar properties as those induced in neurologically normal observers. The theoretical implication is that V1 is not necessary for visual awareness under all circumstances. There are previous reports of patients with unilateral V1 lesions experiencing visual qualia. Hemianopic completion can occur when visual stimuli are presented across the vertical meridian such that one half of the figure falls within the blind hemifield and the other on the sighted field. Some patients are able to perceive the complete figure, including the blind field component, whereas there is no conscious experience when none of the figure intrudes the sighted field (e.g., [8]). There is also prior evidence of TMS-induced percepts in such patients. When TMS was applied over the visual motion area V5/MT+ bilaterally (i.e., both the damaged and intact hemisphere were stimulated with TMS in close temporal proximity), a blindsight subject could perceive bilateral phosphenes [9]. However, in these prior studies, the contribution of the intact hemisphere was required. This was not the case in the study of Mazzi et al., in which qualia could be induced selectively from the ipsilesional hemisphere and experienced exclusively in the blind field. This was not the first attempt to induce phosphenes in patients without V1. In a previous study, application of TMS over the motion-selective area V5/MT in the damaged hemisphere of a blindsight patient did not generate phosphenes [10]. Why the previous attempt failed while Mazzi et al succeeded is an open question. It might relate to the fact that brain lesions are heterogeneous; for example, the patient studied in [10] has lesions beyond V1, including the parietal cortex [11]. Determining the neural correlates of TMS-induced activity and phosphene perception in the absence of V1 by combining TMS with neuroimaging techniques such as EEG or fMRI might help to resolve this discrepancy. The findings of Mazzi et al demonstrate that when V1 is damaged, the affected hemisphere can still generate visual qualia. However, the fact remains that patients with V1
Spotlight lesions are phenomenally blind to visual input. For reasons that require further research, TMS in the study of Mazzi et al. was able to induce the conditions in which visual awareness can arise. What might these conditions be? One possibility is that visual awareness requires inter-areal neural synchrony, established through cortico-cortical feedback (e.g., [12,13,15]), and V1 might be indispensible in this process because it engages in recurrent activity with the majority of extrastriate visual regions [15]. Indeed, V1 is instrumental in enabling normal visual responsiveness to external input throughout the visual cortex; when it is lesioned, extrastriate responses become sluggish, and exhibit abnormally bursty spontaneous activity and high response variability [3,14]. Perhaps inter-areal synchrony cannot arise in the absence of V1, yet it can be artificially induced by TMS, because the application of a TMS pulse simultaneously depolarises a sizeable population of neurons and induces large-scale synchronous neural firing. Furthermore, one might speculate that low-level unconscious visual functions (as found in blindsight) may still be possible in the absence of inter-areal synchrony, in the form of ‘local’ neural readout from individual extrastriate regions [15]. The study of Mazzi et al. sheds new light on the functional role of V1 by demonstrating that this region cannot be the only gateway into visual awareness. However, the fact remains that its lesion abolishes the ability to consciously perceive external visual input. Even though extrastriate regions continue to process visual information in the absence of V1, qualia can be experienced in only very limited circumstances. The challenge now is to decipher those circumstances, as they may give fundamental clues
Trends in Neurosciences November 2014, Vol. 37, No. 11
about the neural processes underlying conscious visual perception. V1 and feedback connections may still be implicated [4–6,13,15]. The question is: how? References 1 Crick, F. and Koch, C. (1995) Are we aware of neural activity in primary visual cortex? Nature 375, 121–123 2 Cowey, A. (2010) The blindsight saga. Exp. Brain Res. 200, 3–24 3 Rodman, H.R. et al. (1989) Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal. J. Neurosci. 9, 2033–2050 4 Stoerig, P. and Cowey, A. (1995) Visual perception and phenomenal consciousness. Behav. Brain Res. 71, 147–156 5 Weiskrantz, L. (1997) Consciousness lost and found, Oxford University Press, (Oxford) 6 Lamme, V.A. (2003) Why visual attention and awareness are different. Trends Cogn. Sci. 7, 12–18 7 Mazzi, C. et al. (2014) Can IPS reach visual awareness without V1? Evidence from TMS in healthy subjects and hemianopic patients. Neuropsychologia 64, 134–144 8 Bender, M.B. and Kahn, R.L. (1949) After-imagery in defective fields of vision. J. Neurol. Neurosurg. Psychiatry 12, 196–204 9 Silvanto, J. et al. (2007) Making the blindsighted see. Neuropsychologia 45, 3346–3350 10 Cowey, A. and Walsh, V. (2000) Magnetically induced phosphenes in sighted, blind and blindsighted observers. Neuroreport 11, 3269–3273 11 Bridge, H. et al. (2008) Changes in connectivity after visual cortical brain damage underlie altered visual function. Brain 131, 1433–1444 12 Dehaene, S. and Changeux, J.P. (2011) Experimental and theoretical approaches to conscious processing. Neuron 70, 200–227 13 Pollen, D.A. (1999) On the neural correlates of visual perception. Cereb. Cortex 9, 4–19 14 Azzopardi, P. et al. (2003) Response latencies of neurons in visual areas MT and MST of monkeys with striate cortex lesions. Neuropsychologia 41, 1738–1756 15 Silvanto, J. (2014) Why is ‘‘blindsight’’ blind?. A new perspective on primary visual cortex, feedback and visual awareness. Conscious. Cogn. http://dx.doi.org/10.1016/j.concog.2014.08.001
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