Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain

Article Information
- Received July 22, 2020
- Revision received December 22, 2020
- Accepted December 23, 2020
- First published March 10, 2021.
- Version of record published March 10, 2021.
Author Information
- 1Department of Psychology, New York University, New York, New York 10003
- 2Department of Philosophy, New York University, New York, New York 10003
- 3Department of Neurology & Neurological Sciences, Stanford University, Stanford, California 94305
- 4School of Medicine, Stanford University, Stanford, California 94305
Author contributions
Author contributions: O.R. conceived of the project; O.R., N.B., and K.C.R.F. contributed to the formulation and writing of the manuscript.
Disclosures
- Received July 22, 2020.
- Revision received December 22, 2020.
- Accepted December 23, 2020.
This work was supported by National Science Foundation Graduate Research Fellowship DGE 1839302 to O.R., and Stanford University School of Medicine Medical Scholars Research Fellowship to K.C.R.F. We thank Richard Brown, Luke Huszar, Aaron Kucyi, Christof Koch, Barbara Montero, Matthias Michel, Rafi Malach, David Poeppel, Josef Parvizi, Moshik Raccah, and Leor Zmigrod for comments on an earlier version of the manuscript.
The authors declare no competing financial interests.
- Correspondence should be addressed to Omri Raccah at or409{at}nyu.edu
Funding
National Science Foundation Graduate Research Fellowship
DGE 1839302
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- RE: Subjective phenomena elicited by intracranial electrical stimulation challenge a global neuronal workspace hypothesisOmri Raccah, Ned Block and Kieran C.R. FoxPublished on: 18 November 2021
- RE: Why intracranial electrical stimulation of the human brain suggests an essential role for prefrontal cortex in conscious processingLionel Naccache, Jean-Pierre Changeux, Theophanis I Panagiotaropoulos and Stanislas DehaenePublished on: 13 September 2021
- RE: Global Workspace Theory (GWT) and prefrontal cortex: A Reply to Raccah et al.Bernard J. Baars, Robert Kozma and Natalie GeldPublished on: 18 May 2021
- Published on: (18 November 2021)Page navigation anchor for RE: Subjective phenomena elicited by intracranial electrical stimulation challenge a global neuronal workspace hypothesisRE: Subjective phenomena elicited by intracranial electrical stimulation challenge a global neuronal workspace hypothesis
- Omri Raccah, PhD Candidate, NSF GRFP Fellow, New York University, Department of Psychology, New York, NY
- Other Contributors:
- Ned Block
- Kieran C.R. Fox
In their commentary (Naccache et al., 2021) on our paper (Raccah et al., 2021), Naccache et al.'s main claim is that the complex and distributed functional organization of the prefrontal cortex (PFC) – relative to sensory cortices – precludes its functional modulation by local intracranial electrical stimulation (iES). Specifically, the authors expect that iES to PFC subregions will produce "a random pattern of activity that does not correspond to any meaningful mental content when applied to PFC." Naccache et al. note that we raise the issue of distributed representation ourselves, but they believe we fail to acknowledge the consequences: "What [Raccah et al.] fail to discuss is that the activation of large vectors of activity, distributed over many neurons, may be needed to elicit a meaningful PFC content." Instead, Naccache et al. suggest that electrical micro-stimulation or optogenetic techniques, in combination with single-unit recordings "should be capable of inducing a predetermined conscious content, better than gross iES."
Our reply both in our original paper (Raccah et al., 2021, p. 2078) and now is that, if global neuronal workspace theory (GNWT) or higher order theories are correct, applying iES to PFC should reliably perturb ongoing perception, e.g. of the doctor's face or what the doctor is saying – but it does not. Naccache et al. are probably correct that iES is too crude to create a meaningful percept ex nihi...
Show MoreIn their commentary (Naccache et al., 2021) on our paper (Raccah et al., 2021), Naccache et al.'s main claim is that the complex and distributed functional organization of the prefrontal cortex (PFC) – relative to sensory cortices – precludes its functional modulation by local intracranial electrical stimulation (iES). Specifically, the authors expect that iES to PFC subregions will produce "a random pattern of activity that does not correspond to any meaningful mental content when applied to PFC." Naccache et al. note that we raise the issue of distributed representation ourselves, but they believe we fail to acknowledge the consequences: "What [Raccah et al.] fail to discuss is that the activation of large vectors of activity, distributed over many neurons, may be needed to elicit a meaningful PFC content." Instead, Naccache et al. suggest that electrical micro-stimulation or optogenetic techniques, in combination with single-unit recordings "should be capable of inducing a predetermined conscious content, better than gross iES."
Our reply both in our original paper (Raccah et al., 2021, p. 2078) and now is that, if global neuronal workspace theory (GNWT) or higher order theories are correct, applying iES to PFC should reliably perturb ongoing perception, e.g. of the doctor's face or what the doctor is saying – but it does not. Naccache et al. are probably correct that iES is too crude to create a meaningful percept ex nihilo, but it is not too crude to perturb an ongoing percept. While it is true that subjective effects in the PFC are especially rare following stimulation relative to the rest of the cortex (Fox et al., 2020), the argument posed by Naccache et al. is simply contradicted by many examples in which local iES to PFC regions produced robust and reproducible effects – except that these effects were not perceptual in nature. In addition to many consistent effects in the orbiotofrontal cortex (OFC) and anterior cingulate cortex (ACC), reproducible effects have been reported in the dorso- and ventro-lateral PFC (Liu et al., 2020; Popa et al., 2016), but these reports were of abstract conceptual thought (consistent with functional neuroimaging evidence; Berkovich-Ohana et al., 2020), rather than perturbations of conscious perception. Notably, this also includes a remarkable variety of motor effects found across PFC subregions (Selimbeyoglu & Parvizi, 2010).
Naccache et al. point to the effects of iES in the ACC and OFC, as predicted by the global neuronal workspace theory. However, the authors give no explanation as to why, if ACC and OFC are part of a general consciousness circuit, stimulation to them does not produce perturbations in visual or auditory experience across dozens of individual cases (Fox et al., 2018; Raccah et al., 2021; Rao et al., 2018; Yih et al., 2019). The GNWT should be able to offer an explanation as to why stimulation to the ACC and OFC produces such a specific group of effects – somatic, visceral, emotional, olfactory – instead of perturbations of ongoing perceptual representations. Critically, these effects are consistent with the known functional roles supported by these regions (Bush et al., 2000; Devinsky et al., 1995; Rolls, 2004). These specialized and consistent iES effects, which are always entirely unrelated to ongoing perceptual content, more likely suggest a link between these local sites and particular conscious content than a constitutive role in consciousness (Malach, 2021).
Naccache et al. note that iES can induce changes in neuronal excitability beyond the stimulation site and suggest that evidence presented in our work is limited by a lack of whole-brain sampling methods: "…while the results compiled by Raccah et al. are of primary importance, the absence of simultaneous recordings of global brain activity elicited by iES is a key limitation of current methods." We agree with Naccache et al. that such methods are critical for inferring regional contributions following stimulation, and will be useful for interpreting iES effects outside the PFC. One could also consider using evoked effective connectivity methods for this purpose (Keller et al., 2014). However, this point is in contradiction with Naccache et al.’s criticism that iES is too crude to elicit effects in the PFC. In our view, the fact that iES has widespread effects, including widespread effects within PFC areas, makes it even more remarkable that there are no reports of changes in ongoing perceptual experience following stimulation to PFC regions.
Notably, Baars and colleagues, who also responded to our work (Baars et al., 2021), state that on their version of global workspace theory (Baars et al., 2013), PFC is not crucial to conscious perception. We identified our targets as including the global neuronal workspace theory (Mashour et al., 2020), a theory that does commit to PFC representation. Naccache et al. are advocates of that theory and one can see from their reply that they retain their commitment to a constitutive role for the PFC in conscious perception.
Understanding the neural basis of human consciousness is perhaps the most difficult challenge in all of science, and we welcome diverse perspectives in this debate. We hope that our synthesis continues to provoke lively discussion and that it might stimulate further research in this domain.
This response can also be found as a preprint: https://osf.io/syn7j/
References
Baars, B. J., Franklin, S., & Ramsøy, T. Z. (2013). Global workspace dynamics: cortical “binding and propagation” enables conscious contents. Frontiers in psychology, 4, 200.
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Baars, B. J., Kozma, R., & Geld, N. (2021). Global workspace theory (GWT) and prefrontal cortex: A reply to Raccah et al. Journal of Neuroscience eLetters.
Berkovich-Ohana, A., Noy, N., Harel, M., Furman-Haran, E., Arieli, A., & Malach, R. (2020). Inter-participant consistency of language-processing networks during abstract thoughts. Neuroimage, 211, 116626.
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Fox, K. C., Shi, L., Baek, S., Raccah, O., Foster, B. L., Saha, S., Margulies, D. S., Kucyi, A., & Parvizi, J. (2020). Intrinsic network architecture predicts the effects elicited by intracranial electrical stimulation of the human brain. Nature human behaviour, 1-14.
Fox, K. C., Yih, J., Raccah, O., Pendekanti, S. L., Limbach, L. E., Maydan, D. D., & Parvizi, J. (2018). Changes in subjective experience elicited by direct stimulation of the human orbitofrontal cortex. Neurology, 91(16), e1519-e1527.
Keller, C. J., Honey, C. J., Entz, L., Bickel, S., Groppe, D. M., Toth, E., Ulbert, I., Lado, F. A., & Mehta, A. D. (2014). Corticocortical evoked potentials reveal projectors and integrators in human brain networks. Journal of Neuroscience, 34(27), 9152-9163.
Liu, A., Friedman, D., Barron, D. S., Wang, X., Thesen, T., & Dugan, P. (2020). Forced conceptual thought induced by electrical stimulation of the left prefrontal gyrus involves widespread neural networks. Epilepsy & Behavior, 104, 106644.
Malach, R. (2021). Local neuronal relational structures underlying the contents of human conscious experience. Neuroscience of Consciousness, 2021(2), niab028.
Mashour, G. A., Roelfsema, P., Changeux, J.-P., & Dehaene, S. (2020). Conscious processing and the global neuronal workspace hypothesis. Neuron, 105(5), 776-798.
Naccache, L., Changeux, J.-P., Panagiotaropoulos, T. I., & Dehaene, S. (2021). Why intracranial electrical stimulation of the human brain suggests an essential role for prefrontal cortex in conscious processing: a commentary on Raccah et al. OSF Preprints.
Naccache, L., Changeux, J.-P., Panagiotaropoulos, T. I., & Dehaene, S. (2021). Why intracranial electrical stimulation of the human brain suggests an essential role for prefrontal cortex in conscious processing: a commentary on Raccah et al. Journal of Neuroscience eLetters.
Popa, I., Donos, C., Barborica, A., Opris, I., Mălîia, M. D., Ene, M., Ciurea, J., & Mîndruţă, I. (2016). Intrusive thoughts elicited by direct electrical stimulation during stereo-electroencephalography. Frontiers in neurology, 7, 114.
Raccah, O., Block, N., & Fox, K. C. (2021). Does the prefrontal cortex play an essential role in consciousness? Insights from intracranial electrical stimulation of the human brain. Journal of Neuroscience, 41(10), 2076-2087.
Rao, V. R., Sellers, K. K., Wallace, D. L., Lee, M. B., Bijanzadeh, M., Sani, O. G., Yang, Y., Shanechi, M. M., Dawes, H. E., & Chang, E. F. (2018, Dec 17). Direct Electrical Stimulation of Lateral Orbitofrontal Cortex Acutely Improves Mood in Individuals with Symptoms of Depression. Curr Biol, 28(24), 3893-3902.e3894.
Rolls, E. T. (2004). The functions of the orbitofrontal cortex. Brain and cognition, 55(1), 11-29.
Selimbeyoglu, A., & Parvizi, J. (2010). Electrical stimulation of the human brain: perceptual and behavioral phenomena reported in the old and new literature. Front Hum Neurosci, 4, 46.
Yih, J., Beam, D. E., Fox, K. C., & Parvizi, J. (2019). Intensity of affective experience is modulated by magnitude of intracranial electrical stimulation in human orbitofrontal, cingulate and insular cortices. Social cognitive and affective neuroscience, 14(4), 339-351.Competing Interests: None declared. - Published on: (13 September 2021)Page navigation anchor for RE: Why intracranial electrical stimulation of the human brain suggests an essential role for prefrontal cortex in conscious processingRE: Why intracranial electrical stimulation of the human brain suggests an essential role for prefrontal cortex in conscious processing
- Lionel Naccache, Professor of Physiology, Neurologist, Cognitive neuroscientist, Sorbonne Université, APHP, Pitié-Salpêtrière, INSERM, Brain Institute (ICM), Paris, France
- Other Contributors:
- Jean-Pierre Changeux
- Theophanis I Panagiotaropoulos
- Stanislas Dehaene
The synthesis by Raccah and colleagues on the perturbations of conscious experience elicited by intracranial electrical stimulation (iES) of the prefrontal cortex (PFC) in awake neurosurgical patients (Raccah, Block et al. 2021) highlights that iES of the PFC shows fewer causal changes of conscious experience than iES of posterior sensory areas. The authors interpreted this finding as a challenge to neuroscientific theories of conscious processing that attribute a central role to PFC, such a Global Neuronal Workspace Theory (GNWT) and Higher Order Thought theory (HOT). We provide here a list of seven major points that begin to specify a GNWT account for the observations compiled by Raccah and colleagues, together with more recent uncited data. The following bullet points are further detailed in our linked preprint (https://osf.io/c96kp/):
1. Do not ‘Abstract’ too far away from the data
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2. The efficacy of iES varies across cortical regions due to differences in local neuronal organization
3. Local stimulation should be enriched by simultaneous global recordings of brain activity
4. Conscious contents can be affected after iES of PFC
5. PFC lesions or PFC trans-cranial magnetic or electric stimulation can alter conscious perception and conscious processing
6. A natural brain stimulation model: Frontal lobe epilepsy does impact conscious content and state
7. Let’s avoid a revival of the famous long...The synthesis by Raccah and colleagues on the perturbations of conscious experience elicited by intracranial electrical stimulation (iES) of the prefrontal cortex (PFC) in awake neurosurgical patients (Raccah, Block et al. 2021) highlights that iES of the PFC shows fewer causal changes of conscious experience than iES of posterior sensory areas. The authors interpreted this finding as a challenge to neuroscientific theories of conscious processing that attribute a central role to PFC, such a Global Neuronal Workspace Theory (GNWT) and Higher Order Thought theory (HOT). We provide here a list of seven major points that begin to specify a GNWT account for the observations compiled by Raccah and colleagues, together with more recent uncited data. The following bullet points are further detailed in our linked preprint (https://osf.io/c96kp/):
1. Do not ‘Abstract’ too far away from the data
2. The efficacy of iES varies across cortical regions due to differences in local neuronal organization
3. Local stimulation should be enriched by simultaneous global recordings of brain activity
4. Conscious contents can be affected after iES of PFC
5. PFC lesions or PFC trans-cranial magnetic or electric stimulation can alter conscious perception and conscious processing
6. A natural brain stimulation model: Frontal lobe epilepsy does impact conscious content and state
7. Let’s avoid a revival of the famous long-lasting misunderstanding of PFC functionsWe agree with Raccah and colleagues to claim that: ‘available data reveals a complex picture that does not provide unequivocal support for either theoretical viewpoint’. But we also tried to show with the help of novel technologies and recent observations why far from being incompatible with current iES evidence, GNWT is already supported by a significant body of experimental data. Future collaborative works using specific topographic micro-stimulation jointly with measures of the propagation of activity to distant sites - should make the data less equivocal.
Show LessCompeting Interests: None declared. - Published on: (18 May 2021)Page navigation anchor for RE: Global Workspace Theory (GWT) and prefrontal cortex: A Reply to Raccah et al.RE: Global Workspace Theory (GWT) and prefrontal cortex: A Reply to Raccah et al.
- Bernard J. Baars, Editor-in-Chief, Society for MindBrain Sciences; Senior Distinguished Fellow,, Center for the Future Mind, Florida Atlantic University, Boca Raton, FL. 80470.
- Other Contributors:
- Robert Kozma
- Natalie Geld
Raccah, Block and Fox (2021) make an incorrect claim about Global Workspace Theory (GWT). GWT does not assert that the prefrontal cortex (PfC) is essential for conscious vision. GWT started in the 1980s as a purely psychological theory of conscious cognition. Based on today's far more detailed understanding of the brain, GWT has adapted to new waves of evidence.
The brain-based version of GWT is called Global Workspace Dynamics (GWD) (Baars et al, 2013; Baars & Geld, 2019), and joins other theories in viewing consciousness as the product of highly integrated and widespread cortico-thalamic (C-T) activity, following a long trail of evidence. GWT-GWD is focused on the entire cerebral cortex, and does not partition cortex into static prefrontal and posterior parts. Rather, the C-T system acts as "a unified oscillatory machine" (Steriade, 1999).
PfC cannot be functionally separated from the rest of the C-T system. Static, gross anatomical divisions are superseded by the dynamical connectome of cortex.
Raccah et al themselves cite evidence that supports the role of PfC in a wide range of conscious contents. These varieties of conscious contents involve PfC and other regions (Dehaene, Kerszberg & Changeux, 1998). Experimental studies have shown that PfC is involved in visual consciousness as well (Kirchner et al; Libedinsky & Livingstone, 2011).
There is a direct causal link between frontal eye fields (FEF) (a region of P...
Show MoreRaccah, Block and Fox (2021) make an incorrect claim about Global Workspace Theory (GWT). GWT does not assert that the prefrontal cortex (PfC) is essential for conscious vision. GWT started in the 1980s as a purely psychological theory of conscious cognition. Based on today's far more detailed understanding of the brain, GWT has adapted to new waves of evidence.
The brain-based version of GWT is called Global Workspace Dynamics (GWD) (Baars et al, 2013; Baars & Geld, 2019), and joins other theories in viewing consciousness as the product of highly integrated and widespread cortico-thalamic (C-T) activity, following a long trail of evidence. GWT-GWD is focused on the entire cerebral cortex, and does not partition cortex into static prefrontal and posterior parts. Rather, the C-T system acts as "a unified oscillatory machine" (Steriade, 1999).
PfC cannot be functionally separated from the rest of the C-T system. Static, gross anatomical divisions are superseded by the dynamical connectome of cortex.
Raccah et al themselves cite evidence that supports the role of PfC in a wide range of conscious contents. These varieties of conscious contents involve PfC and other regions (Dehaene, Kerszberg & Changeux, 1998). Experimental studies have shown that PfC is involved in visual consciousness as well (Kirchner et al; Libedinsky & Livingstone, 2011).
There is a direct causal link between frontal eye fields (FEF) (a region of PfC) and early visual processing. Other varieties of consciousness also appear upon direct stimulation of PfC, as shown by intracranial electrical stimulation (iES). Indeed, state-of-the-art evidence supports a role for PfC in many conscious functions.
It is not fruitful to pose the scientific issues as a contest between PfC and the rest of cortex. The highly connected, recurrent activations of cortex at multiple levels makes the Raccah et al claim unlikely (Kozma & Freeman, 2017).
In summary, consciousness requires a much broader, more integrative view (Bressler & Kelso, 2016). GWT-GWD does not deny the role of local aspects, rather it integrates them at a higher level (Baars et al, 2013; Baars & Geld, 2019).
Mathematically, this has been described as neuropercolation in the cortical neuropil as a phase transition between a basal state consisting of competing, local, fragmented components, and a state of high coherence across the hemisphere globally, when the roles of space and spatial differences cease (Kozma & Puljic, 2015). The transition from fragmented states to global coherence appears to be ignited in areas IT/MTL, in the case of visual consciousness (Dehaene & Changeaux, 2011).
GWT-GWD accounts for an extensive body of evidence, consistent with Edelman's Neural Darwinism, Freeman and Kozma’s Neurodynamics,, Tononi and Koch’s Information Integration Theory, Dehaene and Changeux's Global Neuronal Workspace Theory, Mashour et al, and the functional connectomics of Deco, Vidaurre and Kringelbach.
There is substantial agreement among theories suggesting that the C-T system is inherently dynamic. The claim that the prefrontal cortex is not involved in visual consciousness is therefore unproven. Raccah et al, in fact, provide a wealth of evidence for GWT-GWD; their hypothesis is contradicted by the very evidence they present.
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*This set of theories may be considered similar enough to be treated as a "family" of GW-like approaches, including Deco, Vidaurre & Kringelbach; Edelman, Gally & Baars; and Freeman & Kozma. Each approach is distinctive and each is based on a strong body of evidence; but they converge well.Competing Interests: None declared.