Prefrontal Cortex, Consciousness, and…the Central Sulcus?

The question of whether the prefrontal cortex (PFC) is crucially involved in conscious experience is one that I have been interested in for quite a while. The issue has flared up again recently, especially with the defenders of the Integrated Information Theory of Consciousness defending an anti-PFC account of consciousness (as in Christof Koch’s piece in Nature). I have talked about IIT before (here, here, and here) and I won’t revisit it but I did want to address one issue in Koch’s recent piece. He says,

A second source of insights are neurological patients from the first half of the 20th century. Surgeons sometimes had to excise a large belt of prefrontal cortex to remove tumors or to ameliorate epileptic seizures. What is remarkable is how unremarkable these patients appeared. The loss of a portion of the frontal lobe did have certain deleterious effects: the patients developed a lack of inhibition of inappropriate emotions or actions, motor deficits, or uncontrollable repetition of specific action or words. Following the operation, however, their personality and IQ improved, and they went on to live for many more years, with no evidence that the drastic removal of frontal tissue significantly affected their conscious experience. Conversely, removal of even small regions of the posterior cortex, where the hot zone resides, can lead to a loss of entire classes of conscious content: patients are unable to recognize faces or to see motion, color or space.

So it appears that the sights, sounds and other sensations of life as we experience it are generated by regions within the posterior cortex. As far as we can tell, almost all conscious experiences have their origin there. What is the crucial difference between these posterior regions and much of the prefrontal cortex, which does not directly contribute to subjective content?

The assertion that loss of the prefrontal cortex does not affect conscious experience is one that is often leveled at theories that invoke activity in the prefrontal cortex as a crucial element of conscious experience (like the Global Workspace Theory and the higher-order theory of consciousness in its neuronal interpretation by Hakwan Lau and Joe LeDoux (which I am happy to have helped out a bit in developing)). But this is a misnomer or at least is subject to important empirical objections. Koch does not say which cases he has in mind (and he does not include any references in the Nature paper) but we can get some ideas from a recent exchange in the Journal of Neuroscience.

One case in particular is often cited as evidence that consciousness survives extensive damage to the frontal lobe. In their recent paper Odegaard, Knight, and Lau have argued that this is incorrect. Below is figure 1 from their paper.

Figure 1a from Odegaard, Knight, and Lau

This is brain of Patient A, who was reportedly the first patient to undergo bi-lateral frontal lobectomy.  In it the central sulcus is labeled in red along with Brodman’s areas 4, 6, 9, and 46. Labled in this way it is clear that there is an extensive amount of (the right) prefrontal cortex that is intact (basically everything anterior to area 6 would be preserved PFC). If that were the case then this would hardly be a complete bi-lateral lobectomy! There is more than enough preserved PFC to account for the preserved conscious experience of Patient A.

Boly et al have a companion piece in the journal of neuroscience and a response to the Odegaard paper (Odegaard et al responded to Boly as well and made these same points). Below is figure R1C from the response by Boly et al.

Figure R1C from response by Melanie Boly, Marcello Massimini, Naotsugu Tsuchiya, Bradley R. Postle, Christof Koch, and Giulio Tononi

Close attention to figure R1C shows that Boly et al have placed the central sulcus in a different location than Odegaard et al did. In the Odegaard et al paper they mark the central sulcus behind where the 3,1,2 white numbers occur in the Boly et al image. If Boly et al were correct then, as they assert, pretty much the entire prefrontal cortex is removed in the case of patient A, and if that is the case then of course there is strong evidence that there can be conscious experience in the absence of prefrontal activity.

So here we have some experts in neuroscience, among them Robert T. Knight and Christof Koch, disagreeing about the location of the central sulcus in the Journal of Neuroscience –As someone who cares about neuroscience and consciousness (and has to teach it to undergraduates) this is distressing! And as someone who is not an expert on neurophysiology I tend to go with Knight (surprised? he is on my side, after all!) but even if you are not convinced you should at least be convinced of one thing: it is not clear that there is evidence from “neurological patients in the first half of the 20th century” which suggests that the prefrontal cortex is not crucially involved in conscious experience. What is clear is that is seems a bit odd to keep insisting that there is while ignoring the empirical arguments of experts in the field.

On a different note, I thought it was interesting that Koch made this point.

IIT also predicts that a sophisticated simulation of a human brain running on a digital computer cannot be conscious—even if it can speak in a manner indistinguishable from a human being. Just as simulating the massive gravitational attraction of a black hole does not actually deform spacetime around the computer implementing the astrophysical code, programming for consciousness will never create a conscious computer. Consciousness cannot be computed: it must be built into the structure of the system.

This is a topic for another day but I would have thought you could have integrated information in a simulated system.

8 thoughts on “Prefrontal Cortex, Consciousness, and…the Central Sulcus?

  1. Richard, not sure about the “simulation” argument. If a computer program simulates the function of a kidney, it needs proxies for the input and output of the kidney since the computer program can’t make urine. But if we posit that the input and output of the forebrain is “information” as transmitted by action potentials to and from sensory receptors and motor effectors, this does not pose the same problem as the kidney. the computer doesn’t need proxies for information, since information is what it does. So I don’t think Koch’s argument is convincing.

  2. Dan Pollen, a neurologist, reviewed the literature on frontal damage a number of times in papers in Cerebral Cortex. See for example Pollen, D. A. (2008). “The Fundamental Requirements for Primary Visual Perception.” Cerebral Cortex 18. And Pollen, D. A. (2011). “On the Emergence of Primary Visual Perception.” Cerebral Cortex 21(9): 1941-1953.
    His conclusion was that intact frontal lobes were not necessary for phenomenal consciousness. This is the same view as Koch’s and incompatible with what Hakwan is saying. Still, I think Koch should have said that his reading of the evidence is controversial.

    On why a simulation of a brain on a standard architecture computer would have very low phi: My understanding is that the fact that in the von Neumann architecture all information is funneled through a serial CPU precludes the integration required for significant levels of phi.

  3. Hi Ned and John, thanks for stopping by and commenting!

    Ned, I am aware of Pollen’s work (I actually invited him to be part of the PFC symposium I organized for the ASSC in San Diego but it didn’t work out) but my understanding is that it is based on a literature review (as opposed to examination of patients). That is not terrible but it should be weighted accordingly. And since then we have had updates…one thing I like about the Odegaard et al paper is that they published videos of patients that had only previously circulated informally (I had seen the videos previously because I emailed Bob Knight and asked to view them). The video of the patient with bi-lateral frontal lobectomy who exhibits akenitic mutism is extremely hard to asses. Does he seem to be having conscious experience to you?

    That is interesting re Von Neumann architecture, and I hadn’t thought about that before. Is there anything written on this? It seems the claim is that the computer itself has low phi? But what about the simulated system?

    • “my understanding is that it is based on a literature review (as opposed to examination of patients).” Yes, but Pollen is a neurologist who knows how to read the papers. For example, he knows where the central sulcus is.
      “Does he seem to be having conscious experience to you?” I don’t think anyone can have any idea whether he is having conscious experience from that video. The problem with interpreting bi-lateral frontal lobectomy patients is that the operation destroys the cognitive capacities required for reporting so one doesn’t know what there is to report. But there is a way around that problem: look at varying degrees of frontal damage. Pollen’s point in those papers is that if you look at various different degrees of damage, the picture that emerges is increasing failure to be able to put together a response with increasing damage without any failure to perceive basic properties of color, shape, etc.

      • I agree that there are two issues here. One is the question of whether bi-lateral lobectomy of the frontal lobes affects behavior in a significant way. It does and the traditional cases used to say it doesn’t are suspect (or that is how I interpret the evidence available). I agree it is hard to know what to say about the patient in the video but that is the point! A lot of people have said that removing the prefrontal cortex leaves people for the most part normal (Koch says something like their IQs improve and they go on with their life) and because of this it is supposed to be obvious that consciousness does not depend on activity in the prefrontal cortex (and that we have known this since the 1930s). This conclusion is not supported by the historical evidence (i.e. Patient A) or the current evidence (i.e. the kinds of patients examined by Knight in the video). That doesn’t establish the case one way or the other but it does establish that we shouldn’t make the kinds of arguments that Koch does (not to mention the way in which he asserts that IIT and Global Workspace are the two most popular theories of consciousness).

        The other is whether Koch was in the same position as Pollen was in 2007 and the answer, I would say, is no. Here is a quote from Pollen’s 2007 paper (link here):

        Such capacities in humans are also preserved after extensive bilateral lesions of the prefrontal cortex (Brickner 1936; Damasio 1999). It might be argued that such lesions were not complete enough to exclude a role of these cortices, particularly the dorsolateral prefrontal cortex (Brodmann area 46), in PVP. However, that possibility appears remote given the sparing of the basic visual capacities of psychiatric patients following selective bilateral lesions of prefrontal cortex made with the intent to alleviate severe psychiatric symptoms without impairing the special senses (Heath et al. 1949). Bilateral prefrontal ablations were made in some subjects in Brodmann areas 45 and surrounding cortices, in others in areas 46 and surrounding cortices, and in still other subjects both areas 45 and 46 were bilaterally ablated. No bilateral ablation of prefrontal cortices disrupted basic visual experience for luminance or color and visual fields remained intact.

        Pollen may think the possibly that preserved prefrontal cortex can account for conscious phenomenology of these patients is ‘remote’ but that is based on reports from 1949 and some inferences from other data based on the assumption that prefrontal cortex is not required. But whatever the case about that isn’t this an empirical question? And don’t the arguments in Odegaard et al about this need to be addressed (whether you agree with them or not)? They present some empirical findings which support this ‘remote’ possibility. Pollen didn’t know about them in 2007 but Koch did.

        So, to the third, background question as to whether Pollen was right I would say that we don’t know but the argument should have progressed from historical cases to examination of current lesion data, etc.

  4. Hi Richard, very interesting piece. But I don’t understand the last point you made in the comment. Claiming that the computer itself has a low phi but the simulated system does not sounds to me like saying the human itself has a low phi but his system of thought is highly conscious.

    • Hi Julia, I probably don’t really know what I am talking about but I was thinking that the simulated system (in this case the simulated brain) could be ‘cut’ in the simulation in the same way they do in the actual brain. So, if neuron A is connected to B and C in the simulation then we should be able to disable neuron A and see if any information in the simulated brain is lost, etc. (isn’t one of the goals of simulated brains to do this kind of specific lesion stuff?)…if so then phi could be estimated for it regardless of whether the computer itself had high phi.

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