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Prefrontal lesion evidence against higher-order theories of consciousness

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Abstract

According to higher-order theories of consciousness, a mental state is conscious only when represented by another mental state. Higher-order theories must predict there to be some brain areas (or networks of areas) such that, because they produce (the right kind of) higher-order states, the disabling of them brings about deficits in consciousness. It is commonly thought that the prefrontal cortex produces these kinds of higher-order states. In this paper, I first argue that this is likely correct, meaning that, if some higher-order theory is true, prefrontal lesions should produce dramatic deficits in visual consciousness. I then survey prefrontal lesion data, looking for evidence of such deficits. I argue that no such deficits are to be found, and that this presents a compelling case against higher-order theories.

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Notes

  1. For lucid presentations of the argument just recounted (the so-called simple argument for higher-order theory), see Lycan (2001), Rosenthal (2002). Many, perhaps all, higher-order theorists find this argument compelling (e.g., Gennaro 1996; Carruthers 2000; Kriegel 2009); but see Block (2009), which calls into question the cogency of it.

  2. Higher-order theories can be contrasted with first-order theories of consciousness (Harman 1990; Dretske 1995; Tye 1995), which hold that a first-order representational state can be conscious (whether or not it is targeted by a higher-order state), as long as the first-order state satisfies other conditions (such as being available for use in reasoning and belief-formation).

  3. This is somewhat of a simplification, as Carruthers has sometimes described his theory as a blend of higher-order perception and higher-order thought theories (see his 2004).

  4. Or at least many HO theories. See the discussions below (in Sect. 2.1, and especially Sect. 4.3) concerning how not all HO theories seem equally committed to there being integral areas in the PFC.

  5. There is, for example, something it is like to have pangs of hunger, or to see the red of a firetruck. Experiences like these are what phenomenal consciousness refers to.

  6. For example, some HO theorists will use the terms “experience” or even “what-it’s-like” to describe states that may or may not be phenomenally conscious (e.g., Carruthers 2000). (Byrne does a good job of sorting out the terminological thicket surrounding HO theories; see his 2004.)

  7. For references, see p. 3.

  8. This is still a bit imprecise: If there were more than one network individually sufficient for the production of HO states, then a brain area might fail to be necessary for the having of conscious states, even though it plays an essential role in the production of any number of token conscious states. But the above formulation is sufficient for present purposes.

  9. There is some question as to whether the PFC plays an important role in theory of mind. (For arguments and data in favor of this idea, see Frith and Frith (2003), Gallagher and Frith (2003); for arguments and data against it, see Bird et al. (2004), Saxe et al. (2006).) This could be an issue of consequence: At least one HO theorist (Carruthers 2000) has thought that the theory of mind mechanism might produce (the right kind of) HO states (but see Kriegel 2007). If this were right, and it turned out that the theory of mind mechanism was located entirely outside the PFC, then prefrontal lesion evidence would be less relevant to evaluating HO theories than it is taken to be in this paper.

    This, however, looks like an outlying possibility, as it rests on at least two contentious theses. The first is that the theory of mind mechanism does not depend essentially on structures in the PFC. As just seen, whether or not this is the case is a matter of ongoing debate. The second is that the theory of mind mechanism not only represents others’ mental states, but also one’s own mental states (more specifically, sensory states) (Carruthers 2010). The former, but not the latter, is a function traditionally ascribed to the theory of mind mechanism. Because of the contentiousness of these theses, I leave exploration of this possibility for future research.

  10. It should be mentioned that Baddeley’s theory of working memory is in some danger of being supplanted by a newer theory (Zimmer 2008), one giving less of a central role to the PFC than Baddeley’s. This is not of consequence to present purposes, since Zimmer’s theory still gives the PFC an essential role; meaning that, if the network of brain areas involved in short-term memory constitute an integral network, we should expect deficits in visual consciousness to result when the PFC is damaged.

  11. The primary function of the conceptual short term memory store is to create ‘gists’ of visual scenes: fleeting, conceptual representations of the objects composing one’s current milieu.

  12. Beeckmans makes this identification even in the case of higher-order perception theory (e.g., Lycan 1996). One might wonder if it is apt to identify the production of higher-order perceptions with a conceptual short-term memory system, since some commentators (e.g., Carruthers 2007) have described higher-order perceptions as being nonconceptual. Beeckmans’ reasons for making this identification are complex, and appeal to the specifics of Lycan’s theory. Interested readers should refer to Beeckmans (2007, p. 103).

  13. Or in a parallel case, wherein a lesion to an integral area causes it to only partially lose its ability to produce HO states.

  14. This does raise a question: While it seems true that, if an integral area is damaged, this would result in a dearth of visually conscious states, and it also seems true that this loss would constitute a remarkable change in one’s ongoing visual experience, one might ask: What exactly would this be like, to experience a deficit of visually conscious states? In what remarkable way would this lack of visually conscious states be a departure from what was previously typical of the subject’s ongoing visual experience? For our purposes, we need not answer this question: It is safe to assume that, whatever this would be like, it would constitute some remarkable change in one’s visual experience.

  15. I say that such a change would likely be manifest to the subject, since significant changes in visual consciousness can, in some instances, go unnoticed for a period of time. Subjects suffering from hemianopia (blindness for half the visual field) sometimes will not recognize their visual deficit until they have undergone testing. However, this is not so important for our purposes: When it comes to subjects in the prefrontal lesion data we look at below, it will look very likely that, if the subjects had any striking deficits in visual consciousness, such deficits would be discovered in the course of examination.

  16. It is not always clear whether these researchers think the PFC to be necessary for visual consciousness. When expressing what they think is the relationship between visual consciousness and the PFC, they often put it in terms of the PFC being “critical,” or “essential” for visual consciousness.

  17. I am indebted to Pollen (2008) for calling my attention to some of the PFC lesion studies discussed below.

  18. It is worth noting that one of the patients was Penfield’s sister, and was therefore someone with whom Penfield had frequent and intimate interactions. This makes it seem especially likely that any deficits would have been discovered.

  19. And especially when the supplementary motor area is also damaged (see below).

  20. Akinetic mutism resulting from damage just to the ACC is rare and usually short-lasting. It can also be brought about by damage to subcortical structures connected to the ACC (Mega and Cohenour 1997).

  21. In what particular manner should we expect the deficits to be detected? I do not precisely know, but one could guess that a subject with a disabled integral area would not perform normally on (at least some) tests of their visual abilities. Failing that, we could probably still expect the subject to volunteer information indicating that things “seemed” visually different to her.

  22. The location of the lesions differed from subject to subject.

  23. As discussed in fn. 14, something I am not speculating on is exactly what kinds of changes we would expect. Perhaps the subjects would find even non-masked stimuli hard to see. Perhaps they would balk at even attempting the task, because it would phenomenologically seem to them as if they were blind, or mostly blind. I am not sure of any of this. What I am certain of is that we would expect deficits of a magnitude greater than those seen in this experiment.

  24. A magnetic field is used to temporarily take “off-line” one or more brain areas.

  25. There is another lesion case some HO theorists (Lau and Rosenthal) have thought to support HO theories: At the 14th annual meeting of the Association for the Scientific Study of Consciousness (June 2010, Toronto), neuroscientist Robert Knight briefly discussed a subject with large bilateral prefrontal lesions who was only minimally responsive to stimuli. However, since this is an unpublished study, many relevant details are unavailable, making it difficult to say anything with confidence about what it means for HO theories. Nonetheless, my guess would be that such a study fails to support HO theories for reasons similar to why the case of akinetic mutism does (see Sect. 3.1).

  26. GY is probably the blindsighted subject who has been most thoroughly studied; see Weiskrantz (1997).

  27. For reviews of data suggesting a close relationship between the PFC and visual consciousness, see Rees et al. (2002), Dehaene and Changeux (2011).

  28. Given certain background systems are functioning normally, such as areas in the upper brain stem and thalamus; see Block (2009) for discussion.

  29. This is to say that the network of areas does not contain, as an essential component, any area in the PFC (see Sect. 2.1).

  30. Naturally, this objection might not get off the ground in the case of the patient who had his entire PFC removed (Sect. 3.1), but I put this aside in considering the objection.

  31. This idea of redundancy would need modification were we to consider an (at least superficially) different version of HO theory, in which it is but one HO state providing for all of a subject’s conscious states. (Instead of a large number of HO states, there would be just one HO state with complex contents.) In this case, the redundancy of representation all happens within the same HO state: Different components of the HO state would have the same lower-order state as their content.

  32. It is also possible that the extra integral area never redundantly represented the lower-order states, but rather came on-line only after the first integral area was damaged (it being a “back up” system of sorts). Instances in which one brain area takes on the function of another are examples of “neuroplasticity” (Grafman 2000). I postpone consideration of neuroplasticity until the next subsection.

  33. Or just one HO state with very complex contents (see fn. 31).

  34. This is, in fact, Carruthers’ primary motivation for adopting a dispositionalist form of HO theory, according to which a mental state is conscious even if there is merely a disposition for an HO state to be formed about that mental state.

  35. It has been argued that our visual phenomenology is not as rich as it seems (Dennett 1991; O’Regan 1992; Simons 2000; but see Block 2001), and some HO theorists have availed themselves of these arguments in hopes of minimizing the amount of HO states required for the typical visual experience (Weisberg 1999; Gennaro 2004; but see Carruthers 2000, pp. 299–301). Perhaps a similar strategy could be successfully adopted in response to the problem of redundant representation that I have raised here, but this remains to be seen.

  36. Note that, in such a scenario, if the lesioned area was an integral area, we would expect the subject both to experience deficits in visual consciousness (she would have lost the ability to produce HO states in the same quantity), and have the ability to report that she was experiencing such deficits; thereby allowing her condition to be discovered.

  37. Flohr offers a neurologically based version of HO theory, one appearing not to necessarily implicate the PFC. The theory is pitched at the neuronal level, hypothesizing the NMDA synapse to be what ultimately enables building “higher-order, self-reflexive representational structures” (1999, p. 255). The NMDA synapse is qualified to do this, argues Flohr, because of its ability to produce both transient and permanent changes in synaptic weights. Given that the theory is (for the most part) based at the neuronal level, it appears not wed to it being any particular brain areas that produce the HO states, and therefore presents one promising avenue for the HO theorist to explore.

  38. Here, in their own words, is how these philosophers describe an HO thought: According to Rosenthal, “a mental state is conscious just in case it is accompanied by a non-inferential…assertoric thought to the effect that one is in that very state” (2002, p. 410). Carruthers holds that conscious states must be disposed to bring about an “activated belief (possibly a non-conscious one) that I have M, and to cause it non-inferentially” (2000, p. 227). Gennaro says that an HO thought is “the thought ‘that I am in M’…What exactly is its content? Of course it involves reference to a subject (‘I’) and to a mental state (‘M’)” (1993, p. 58).

  39. Some HO thought theorists have attempted to minimize this conclusion (see Gennaro 1993, 1996; Rosenthal 2002), this being an attempt to respond to philosophers who have argued that, if HO thought theory was true, then infants and animals would not be conscious, since these beings lack the cognitive sophistication required for HO thoughts (Carruthers 1989, 1992, 1999; Dretske 1995; Tye 1995). Generally speaking, the HO thought theorists in question have argued that the concepts used in an HO thought can be rather crude, including the concept of oneself, and so producing HO thoughts is not as cognitively demanding as we might first think.

    I think the arguments these HO theorists have offered do not make it look as if there could be areas outside the PFC that are able to produce HO thoughts. While not having space to go into this, I will nonetheless note that nothing these HO thought theorists have said so far chips away at the most cognitively-demanding aspect of an HO thought, which is its complexity: An HO thought is a representation in which a mental state is represented as being a state of oneself.

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Acknowledgments

I would like to thank Uriah Kriegel and Shaun Nichols for comments on earlier drafts of this paper, and Rocco Gennaro, Hakwan Lau, Brian Fiala, and numerous others for illuminating discussions on this topic.

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Kozuch, B. Prefrontal lesion evidence against higher-order theories of consciousness. Philos Stud 167, 721–746 (2014). https://doi.org/10.1007/s11098-013-0123-9

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