Electrical Stimulation of Human Fusiform Face-Selective Regions Distorts Face Perception

Josef Parvizi; Corentin Jacques; Brett L. Foster; Nathan Withoft; Vinitha Rangarajan; Kevin S. Weiner; Kalanit Grill-Spector

doi:10.1523/JNEUROSCI.2609-12.2012

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Re:Responses in the Fusiform Face Area do not cause conscious face perception
Josef Parvizi

Submitted on: 27 December 2012
Responses in the Fusiform Face Area do not cause conscious face perception
Johannes J. Fahrenfort

Submitted on: 21 December 2012

Submitted on: (27 December 2012)

Re:Responses in the Fusiform Face Area do not cause conscious face perception
Josef Parvizi
We thank Fahrenfort and van Gaal for their feedback and for reminding us that our statement about causality may need clarification to prevent misinterpretations.
We agree that face selective responses in fusiform gyrus (FG) are not equal to the subjective awareness of faces. Based on our findings, we did not claim that face-selective activations in FG were sufficient for face perception. As we stated in our orig...
Show More

We thank Fahrenfort and van Gaal for their feedback and for reminding us that our statement about causality may need clarification to prevent misinterpretations.
We agree that face selective responses in fusiform gyrus (FG) are not equal to the subjective awareness of faces. Based on our findings, we did not claim that face-selective activations in FG were sufficient for face perception. As we stated in our original paper, "our findings provide evidence for the causal role of these fusiform face-selective regions in face perception". Attributing a causal role in face perception does not imply that the perception of faces reside in the FG sites alone, nor does it imply that the activity of these regions is sufficient for conscious awareness of faces. That is why we stated in our paper that although our findings "clearly suggest face-selective perceptual processing in the FG, we are mindful that they do not explain the exact nature of such processing".
Given that each cortical site is connected with a specific network of cortical and subcortical regions, we suggested that the injected electrical current in our study might have affected the local activity in the FG as well as activity of a selective neuroanatomical network connected to it. As we have stated previously (Selimbeyoglu and Parvizi, 2010), as well as in our paper, "disruption in neural activity caused by electrical brain stimulation occurs by driving current into a large neural population under each electrode, ... which in turn affects local responses, as well as distal cortical and subcortical sites via propagation of current along the afferent and efferent axons of this neuronal population". (See for example, Logothetis et al., 2010). Therefore, any perceptual or behavioral effect of the injected electricity in the FG could be attributed to the involvement of its selective neuroanatomical network, (which may even include subcortical nodes, see also (Parvizi, 2009). That is why we stated that our observations could be attributed to "local responses [in the FG], as well as distal cortical and subcortical sites via propagation of [electrical] current along the afferent and efferent axons of [FG] neuronal population." This led us to suggest the presence of a "face-selective network", as we stated in our paper, "the existence of a specific neural circuit involved in visual perception of faces." In line with Fahrenfort and van Gaal's comments, we believe that future studies utilizing additional methods, may be able to tease apart the specific contribution of each node of this network in face perception, as we have written explicitly, "future studies with methods affecting only local neuronal responses (e.g., by cooling electrodes) will provide additional evidence of the contribution of local neural responses within these sites during the conscious perception of faces".
Our data adds to a large body of evidence that responses in the FG (but not early visual cortex) are higher when people perceive faces than when they do not (Hasson et al., 2001; Moutoussis and Zeki, 2002; Grill- Spector et al., 2004), and that lesions to the FG (Damasio et al., 1982; Barton, 2008) lead to inability to perceive faces whereas lesions to early visual cortex and the retina lead to blindness.
Josef Parvizi and Kalanit Grill-Spector
Barton JJ (2008) Structure and function in acquired prosopagnosia: lessons from a series of 10 patients with brain damage. J Neuropsychol 2:197-225.
Damasio AR, Damasio H, Van Hoesen GW (1982) Prosopagnosia: anatomic basis and behavioral mechanisms. Neurology 32:331-341.
Grill-Spector K, Knouf N, Kanwisher N (2004) The fusiform face area subserves face perception, not generic within-category identification. Nat Neurosci 7:555-562.
Hasson U, Hendler T, Ben Bashat D, Malach R (2001) Vase or face? A neural correlate of shape-selective grouping processes in the human brain. J Cogn Neurosci 13:744-753.
Logothetis NK, Augath M, Murayama Y, Rauch A, Sultan F, Goense J, Oeltermann A, Merkle H (2010) The effects of electrical microstimulation on cortical signal propagation. Nat Neurosci 13:1283-1291.
Moutoussis K, Zeki S (2002) The relationship between cortical activation and perception investigated with invisible stimuli. Proc Natl Acad Sci U S A 99:9527-9532.
Parvizi J (2009) Corticocentric myopia: old bias in new cognitive sciences. Trends Cogn Sci 13:354-359.
Selimbeyoglu A, Parvizi J (2010) Electrical stimulation of the human brain: perceptual and behavioral phenomena reported in the old and new literature. Frontiers in human neuroscience 4:46.
Show Less

Competing Interests: None declared.
Submitted on: (21 December 2012)

Responses in the Fusiform Face Area do not cause conscious face perception
Johannes J. Fahrenfort, Assistant Professor
Other Contributors:
Simon van Gaal
This study described what happens when the right fusiform gyrus (FG) is stimulated in -vivo using Electrical Brain Stimulation (EBS) (Parvizi et al., 2012). Concurrent EBS of mFus and pFus (mid and posterior FG) induced a face- specific perceptual distortion, prompting these authors to conclude a causal role of FG in face perception. This finding is in agreement with a Nature study that showed that stimulating face-select...
Show More

This study described what happens when the right fusiform gyrus (FG) is stimulated in -vivo using Electrical Brain Stimulation (EBS) (Parvizi et al., 2012). Concurrent EBS of mFus and pFus (mid and posterior FG) induced a face- specific perceptual distortion, prompting these authors to conclude a causal role of FG in face perception. This finding is in agreement with a Nature study that showed that stimulating face-selective cells in inferotemporal cortex of awake monkey prompted a preference for behavioral face responses (Afraz et al., 2006). Although both results are highly interesting, they do not warrant the conclusion that face-selective regions cause face perception. Alternatively, face-selective activations are necessary, but not sufficient for face perception. By analogy, subretinal stimulation has a massive influence on visual perception (Zrenner et al., 2011), but few will claim that the retina causes visual perception.
Indeed, a recent study by Ku and colleagues showed that face- selective activity is preserved in anaesthetized monkeys (Ku et al., 2011). Moreover, Moutoussis and Zeki (Moutoussis and Zeki, 2002) have shown that faces that are rendered invisible using dichoptic fusion still produce face-selective FG responses. Recently, we have replicated and extended this result by confirming the presence of visibility invariant FG face-tuning (Fahrenfort et al., 2012). Crucially however, we also show that cortico-cortical integration across face-specific regions and early visual cortex is more indicative of conscious face perception than face- selectivity itself. This suggests that stimulating face-selective cells encroaches upon processes of cortico-cortical integration, rather than causing conscious face perception in isolation. To conclude that face- selective regions are causal in bringing about face perception requires proof that stimulating face-selective regions produces face perception in the absence of interactions with other visual areas (e.g. by removal or inactivation of these areas).
Johannes J. Fahrenfort and Simon van Gaal
Afraz SR, Kiani R, Esteky H (2006) Microstimulation of inferotemporal cortex influences face categorization. Nature 442:692-695.
Fahrenfort J, Snijders TM, Heinen K, van Gaal S, Scholte HS, Lamme VAF (2012) Neuronal integration in visual cortex elevates face category tuning to conscious face perception. P Natl Acad Sci USA.
Ku SP, Tolias AS, Logothetis NK, Goense J (2011) FMRI of the face- processing network in the ventral temporal lobe of awake and anesthetized macaques. Neuron 70:352-362.
Moutoussis K, Zeki S (2002) The relationship between cortical activation and perception investigated with invisible stimuli. P Natl Acad Sci USA 99:9527-9532.
Parvizi J, Jacques C, Foster BL, Withoft N, Rangarajan V, Weiner KS, Grill-Spector K (2012) Electrical stimulation of human fusiform face- selective regions distorts face perception. J Neurosci 32:14915-14920.
Zrenner E, Bartz-Schmidt KU, Benav H, Besch D, Bruckmann A, Gabel VP, Gekeler F, Greppmaier U, Harscher A, Kibbel S, Koch J, Kusnyerik A, Peters T, Stingl K, Sachs H, Stett A, Szurman P, Wilhelm B, Wilke R (2011) Subretinal electronic chips allow blind patients to read letters and combine them to words. P R Soc B 278:1489-1497.
Conflict of Interest:
None declared
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Competing Interests: None declared.

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Re:Responses in the Fusiform Face Area do not cause conscious face perception
Josef Parvizi

Published on: 27 December 2012
Responses in the Fusiform Face Area do not cause conscious face perception
Johannes J. Fahrenfort

Published on: 21 December 2012

Published on: (27 December 2012)

Re:Responses in the Fusiform Face Area do not cause conscious face perception
Josef Parvizi
We thank Fahrenfort and van Gaal for their feedback and for reminding us that our statement about causality may need clarification to prevent misinterpretations.
We agree that face selective responses in fusiform gyrus (FG) are not equal to the subjective awareness of faces. Based on our findings, we did not claim that face-selective activations in FG were sufficient for face perception. As we stated in our orig...
Show More

We thank Fahrenfort and van Gaal for their feedback and for reminding us that our statement about causality may need clarification to prevent misinterpretations.
We agree that face selective responses in fusiform gyrus (FG) are not equal to the subjective awareness of faces. Based on our findings, we did not claim that face-selective activations in FG were sufficient for face perception. As we stated in our original paper, "our findings provide evidence for the causal role of these fusiform face-selective regions in face perception". Attributing a causal role in face perception does not imply that the perception of faces reside in the FG sites alone, nor does it imply that the activity of these regions is sufficient for conscious awareness of faces. That is why we stated in our paper that although our findings "clearly suggest face-selective perceptual processing in the FG, we are mindful that they do not explain the exact nature of such processing".
Given that each cortical site is connected with a specific network of cortical and subcortical regions, we suggested that the injected electrical current in our study might have affected the local activity in the FG as well as activity of a selective neuroanatomical network connected to it. As we have stated previously (Selimbeyoglu and Parvizi, 2010), as well as in our paper, "disruption in neural activity caused by electrical brain stimulation occurs by driving current into a large neural population under each electrode, ... which in turn affects local responses, as well as distal cortical and subcortical sites via propagation of current along the afferent and efferent axons of this neuronal population". (See for example, Logothetis et al., 2010). Therefore, any perceptual or behavioral effect of the injected electricity in the FG could be attributed to the involvement of its selective neuroanatomical network, (which may even include subcortical nodes, see also (Parvizi, 2009). That is why we stated that our observations could be attributed to "local responses [in the FG], as well as distal cortical and subcortical sites via propagation of [electrical] current along the afferent and efferent axons of [FG] neuronal population." This led us to suggest the presence of a "face-selective network", as we stated in our paper, "the existence of a specific neural circuit involved in visual perception of faces." In line with Fahrenfort and van Gaal's comments, we believe that future studies utilizing additional methods, may be able to tease apart the specific contribution of each node of this network in face perception, as we have written explicitly, "future studies with methods affecting only local neuronal responses (e.g., by cooling electrodes) will provide additional evidence of the contribution of local neural responses within these sites during the conscious perception of faces".
Our data adds to a large body of evidence that responses in the FG (but not early visual cortex) are higher when people perceive faces than when they do not (Hasson et al., 2001; Moutoussis and Zeki, 2002; Grill- Spector et al., 2004), and that lesions to the FG (Damasio et al., 1982; Barton, 2008) lead to inability to perceive faces whereas lesions to early visual cortex and the retina lead to blindness.
Josef Parvizi and Kalanit Grill-Spector
Barton JJ (2008) Structure and function in acquired prosopagnosia: lessons from a series of 10 patients with brain damage. J Neuropsychol 2:197-225.
Damasio AR, Damasio H, Van Hoesen GW (1982) Prosopagnosia: anatomic basis and behavioral mechanisms. Neurology 32:331-341.
Grill-Spector K, Knouf N, Kanwisher N (2004) The fusiform face area subserves face perception, not generic within-category identification. Nat Neurosci 7:555-562.
Hasson U, Hendler T, Ben Bashat D, Malach R (2001) Vase or face? A neural correlate of shape-selective grouping processes in the human brain. J Cogn Neurosci 13:744-753.
Logothetis NK, Augath M, Murayama Y, Rauch A, Sultan F, Goense J, Oeltermann A, Merkle H (2010) The effects of electrical microstimulation on cortical signal propagation. Nat Neurosci 13:1283-1291.
Moutoussis K, Zeki S (2002) The relationship between cortical activation and perception investigated with invisible stimuli. Proc Natl Acad Sci U S A 99:9527-9532.
Parvizi J (2009) Corticocentric myopia: old bias in new cognitive sciences. Trends Cogn Sci 13:354-359.
Selimbeyoglu A, Parvizi J (2010) Electrical stimulation of the human brain: perceptual and behavioral phenomena reported in the old and new literature. Frontiers in human neuroscience 4:46.
Show Less

Competing Interests: None declared.
Published on: (21 December 2012)

Responses in the Fusiform Face Area do not cause conscious face perception
Johannes J. Fahrenfort, Assistant Professor
Other Contributors:
Simon van Gaal
This study described what happens when the right fusiform gyrus (FG) is stimulated in -vivo using Electrical Brain Stimulation (EBS) (Parvizi et al., 2012). Concurrent EBS of mFus and pFus (mid and posterior FG) induced a face- specific perceptual distortion, prompting these authors to conclude a causal role of FG in face perception. This finding is in agreement with a Nature study that showed that stimulating face-select...
Show More

This study described what happens when the right fusiform gyrus (FG) is stimulated in -vivo using Electrical Brain Stimulation (EBS) (Parvizi et al., 2012). Concurrent EBS of mFus and pFus (mid and posterior FG) induced a face- specific perceptual distortion, prompting these authors to conclude a causal role of FG in face perception. This finding is in agreement with a Nature study that showed that stimulating face-selective cells in inferotemporal cortex of awake monkey prompted a preference for behavioral face responses (Afraz et al., 2006). Although both results are highly interesting, they do not warrant the conclusion that face-selective regions cause face perception. Alternatively, face-selective activations are necessary, but not sufficient for face perception. By analogy, subretinal stimulation has a massive influence on visual perception (Zrenner et al., 2011), but few will claim that the retina causes visual perception.
Indeed, a recent study by Ku and colleagues showed that face- selective activity is preserved in anaesthetized monkeys (Ku et al., 2011). Moreover, Moutoussis and Zeki (Moutoussis and Zeki, 2002) have shown that faces that are rendered invisible using dichoptic fusion still produce face-selective FG responses. Recently, we have replicated and extended this result by confirming the presence of visibility invariant FG face-tuning (Fahrenfort et al., 2012). Crucially however, we also show that cortico-cortical integration across face-specific regions and early visual cortex is more indicative of conscious face perception than face- selectivity itself. This suggests that stimulating face-selective cells encroaches upon processes of cortico-cortical integration, rather than causing conscious face perception in isolation. To conclude that face- selective regions are causal in bringing about face perception requires proof that stimulating face-selective regions produces face perception in the absence of interactions with other visual areas (e.g. by removal or inactivation of these areas).
Johannes J. Fahrenfort and Simon van Gaal
Afraz SR, Kiani R, Esteky H (2006) Microstimulation of inferotemporal cortex influences face categorization. Nature 442:692-695.
Fahrenfort J, Snijders TM, Heinen K, van Gaal S, Scholte HS, Lamme VAF (2012) Neuronal integration in visual cortex elevates face category tuning to conscious face perception. P Natl Acad Sci USA.
Ku SP, Tolias AS, Logothetis NK, Goense J (2011) FMRI of the face- processing network in the ventral temporal lobe of awake and anesthetized macaques. Neuron 70:352-362.
Moutoussis K, Zeki S (2002) The relationship between cortical activation and perception investigated with invisible stimuli. P Natl Acad Sci USA 99:9527-9532.
Parvizi J, Jacques C, Foster BL, Withoft N, Rangarajan V, Weiner KS, Grill-Spector K (2012) Electrical stimulation of human fusiform face- selective regions distorts face perception. J Neurosci 32:14915-14920.
Zrenner E, Bartz-Schmidt KU, Benav H, Besch D, Bruckmann A, Gabel VP, Gekeler F, Greppmaier U, Harscher A, Kibbel S, Koch J, Kusnyerik A, Peters T, Stingl K, Sachs H, Stett A, Szurman P, Wilhelm B, Wilke R (2011) Subretinal electronic chips allow blind patients to read letters and combine them to words. P R Soc B 278:1489-1497.
Conflict of Interest:
None declared
Show Less

Competing Interests: None declared.

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