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Dual Perspectives

Should a Few Null Findings Falsify Prefrontal Theories of Conscious Perception?

Brian Odegaard, Robert T. Knight and Hakwan Lau
Journal of Neuroscience 4 October 2017, 37 (40) 9593-9602; https://doi.org/10.1523/JNEUROSCI.3217-16.2017
Brian Odegaard
1Department of Psychology, University of California, Los Angeles, California 90095-1563,
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Robert T. Knight
2Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720,
3Department of Psychology, University of California, Berkeley 94720,
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Hakwan Lau
1Department of Psychology, University of California, Los Angeles, California 90095-1563,
4Brain Research Institute, University of California, Los Angeles, California 90095, and
5Department of Psychology, University of Hong Kong, Pokfulam Road, Hong Kong
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    Figure 1.

    The brain of Patient A following “bilateral” frontal lobectomy (data from Brickner, 1952). Patient A was reported as the first human subject to undergo “bilateral” frontal lobectomy. Although this patient has previously been described as a classic example of how lesions to PFC do not impair consciousness (Koch et al., 2016a), simple visual inspection of this patient's postmortem brain image reveals that massive amounts of residual right PFC remained following the surgery. Therefore, the fact that this patient exhibited signs of consciousness following surgery is not surprising. This patient also had a large posterior meningioma exerting pressure on extrastriate cortices. The green region marks the posterior meningioma, the red line labels the central sulcus, the yellow line shows the Sylvian fissure, and the blue arrow marks the temporal tip. Brodmann areas are marked by white numbers.

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    Figure 2.

    Relationships between cortical lesions and general awareness of the external world. Shown here are schematic depictions of typical lesion locations for each of the following types of impairments. A, Bilateral occipital lesions can cause cortical blindness (Melnick et al., 2016) but preserve an individual's general awareness of the surrounding world, via other sensory modalities. B, Bilateral parietal lesions can cause Balint's syndrome, typically characterized by an inability to perceive multiple objects in the visual field coherently, but again, this leaves basic sensory awareness intact. C, Bilateral orbitofrontal lesions cause problems with social regulation, but not sensory perception or consciousness. D, Patients with bilateral lateral PFC lesions are “conscious” in the sense that they are “awake,” as opposed to being in a coma, but they lack the ability to engage meaningfully with the external world with a normal level of conscious awareness. Extensive unilateral PFC lesions do not tend to cause these symptoms, highlighting that one functional side of PFC may be sufficient to support general conscious behavior. However, further psychophysical evidence indicates that even unilateral PFC lesioned patients may suffer from specific impoverishment of subjective perceptual experiences (Del Cul et al., 2009; Fleming et al., 2014).

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    Figure 3.

    Lesion to PFC specifically impairs subjective perceptual introspection. In a study by Fleming et al. (2014), healthy controls (HC), patients with lesions to anterior PFC (aPFC), and patients with temporal lobe lesions (TL) were tested in a perception task and a memory task. A, Overall task performance was equivalent across the three different groups in both tasks. B, Displayed here (meta-d′/d′) is a measure of the meaningfulness of subjective confidence ratings; that is, the degree to which they distinguish between correct and incorrect judgments, expressed on a scale where 1 implies statistical optimality and 0 indicates chance-level trial-by-trial correspondence between confidence and accuracy (Maniscalco and Lau, 2012). This measure showed a nearly 50% decrease in patients with aPFC lesions, compared with patients with temporal lesions and healthy controls, and this effect was specific to perception rather than memory. **P < 0.01; *P < 0.05; n.s. = not significant.

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    Figure 4.

    PFC activity represents specific perceptual content, even when it is not relevant to current tasks. In a multiunit recording study (Mante et al., 2013), monkeys had to make saccades to indicate either the direction or the color of the majority of moving dots, depending on the fixation cue. Task-irrelevant/unattended information (e.g., color) was decodable from neuronal activity in the frontal eye field, almost as well as task-relevant information (e.g., motion).

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    Figure R1.

    Annotated postmortem anatomy for Patient A (Brickner, 1952). A, Anatomical definition of cerebral sulci according to a standard neurosurgical postmortem atlas (Ono et al., 1990). Labels refer to: a: central sulcus; b: Sylvian fissure; c: precentral sulcus; d: superior frontal sulcus; e: inferior frontal sulcus; f: postcentral sulcus; g: intraparietal sulcus. B, Lateral view of Patient A's brain, with blue lines highlighting central and precentral sulci as well as Sylvian fissure as defined in A. Digits refer to Brodmann areas. The posterior cut performed during surgery, just anterior to area 6, is illustrated with an orange dashed line; dural membranes adhere to the damaged brain. C, Postero-lateral view displayed in Odegaard et al. (2017), which shows preserved Brodmann areas 4 and 6.

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    Patient with bilateral lateral PFC lesions (impaired consciousness). A lateral case: this patient sustained extensive bilateral infarctions of lateral prefrontal cortex over a one month period due to emboli from the heart.

  • Movie 2.

    Patient with bilateral orbitofrontal lesions (conscious). An orbital case: this patient ran a scooter into a pole, with extensive bilateral damage to orbitofrontal cortex.

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The Journal of Neuroscience: 37 (40)
Journal of Neuroscience
Vol. 37, Issue 40
4 Oct 2017
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Should a Few Null Findings Falsify Prefrontal Theories of Conscious Perception?
Brian Odegaard, Robert T. Knight, Hakwan Lau
Journal of Neuroscience 4 October 2017, 37 (40) 9593-9602; DOI: 10.1523/JNEUROSCI.3217-16.2017

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Should a Few Null Findings Falsify Prefrontal Theories of Conscious Perception?
Brian Odegaard, Robert T. Knight, Hakwan Lau
Journal of Neuroscience 4 October 2017, 37 (40) 9593-9602; DOI: 10.1523/JNEUROSCI.3217-16.2017
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  • Article
    • Abstract
    • An opportunity to empirically resolve some enduring controversies
    • The clinical neuropsychology of consciousness: “classical” case studies
    • How do lesions to PFC specifically affect subjective perception?
    • Does PFC activity reflect specific perceptual content?
    • Is PFC activity only related to explicit perceptual reports?
    • Footnotes
    • References
    • Response from Dual Perspectives Companion Authors–Melanie Boly, Marcello Massimini, Naotsugu Tsuchiya, Bradley R. Postle, Christof Koch, and Giulio Tononi Some of the arguments raised by Odegaard et al. deserve a brief discussion. Clinical neuropsychology
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Keywords

  • attention
  • awareness
  • consciousness
  • metacognition
  • prefrontal cortex

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