Afterimages: A Tool for Defining the Neural Correlate of Visual Consciousness

OPINION article Front. Hum. Neurosci., 19 July 2013Sec. Cognitive Neuroscience Volume 7 - 2013 | https://doi.org/10.3389/fnhum.2013.00387

'Self' and the Problem of Consciousness

Chapter 16 - The Neural Correlates of Consciousness

This thesis addresses the question of whether people actually see the same visual stimuli somehow differently, and under what conditions, if so. It is an experimental contribution to the basic understanding of visual and especially face perception, and its neural correlates, with an emphasis on comparing patterns of neural activity driven by visual stimuli across trials and across individuals. We make extensive use of functional magnetic resonance imaging (fMRI); all inferences about neural activity are made via this intermediary. The thesis is organized into two parts: In Part I, we investigate the nature of face familiarity and distinctiveness at perceptual and neural levels. We first address the question of how the faces of those people personally familiar to a viewer appear different than they would to an unfamiliar viewer. The main result is that they appear more distinctive, i.e., dissimilar to and distinguishable from other faces, and more so the higher the level of familiarity. Having established this connection between face familiarity and distinctiveness, we ask next what is different about the perception of such faces, as compared with indistinct and unfamiliar faces, at the level of brain activation. We find that familiar and distinctive faces are represented more consistently: compared with indistinct faces, which evoke slightly different patterns of activity with each new presentation, these faces evoke slightly similar patterns. Combined with the observation that consistency can enhance memory encoding (a result reported by Xue et al. [102]), this suggests a cyclic process for the learning of unfamiliar faces in which consistent representation and the presence of newly formed memories mutually feedback on each other. Whereas in Part I we focus on individual differences in neural activity, principally by experimentally manipulating stimulus familiarity, in Part II, we shift our focus to similarities across individuals and extend our investigation beyond faces to the perception of visual objects in general and moving images. We begin with an experiment involving the perception of static images selected from 44 object categories, where we find that the distances between these categories, induced from activity in cortical visual object areas, correlate highly between subjects, and also to distances inferred from a behavioral clustering task, and that this correlation remains significant even among subsets of closely related categories. We also show that one subject's brain activity can be accurately modeled using another's, and that this allows us to predict which image a subject is viewing based on his/her brain activity. Then, in a different experiment investigating the perception of dynamic/video stimuli, we find evidence that when watching videos with sound, visual attention is likely blurred at times and transferred to audition; subjects relatively temporally decorrelate in visual areas compared to the muted case, in which the patterns of neural activity correlate across subjects at an average of 78% the level found with oneself later in time. The findings reported in this thesis thus offer quantitative lower bounds on how similarly different individuals neurally experience visual stimuli, and an explanation for how they perceptually and neurally diverge when familiarity with a (face) stimulus varies, suggesting a possible mechanism for the encoding of new visual objects into memory. We conclude with a discussion of some of the questions raised by this work and directions for future research.

Recent findings in neuroscience strongly suggest that an object's features (e.g., its color, texture, shape, etc.) are represented in separate areas of the visual cortex. Although represented in separate neuronal areas, somehow the feature representations are brought together as a single, unified object of visual consciousness. This raises a question of binding: how do neural activities in separate areas of the visual cortex function to produce a feature-unified object of visual consciousness? Several prominent neuroscientists have adopted neural synchrony and attention-based approaches to explain object feature binding. I argue that although neural synchrony and/or attentional mechanisms might function to disambiguate an object's features, it is difficult to see how either of these mechanisms could fully explain the unity of an object's features at the level of visual consciousness. After presenting a detailed critique of neural synchrony and attention-based approaches to object feature binding, I propose interactive hierarchical structuralism (IHS) . This view suggests that a unified percept (i.e., a feature-unified object of visual consciousness) is not reducible to the activity of any cognitive capacity or to any localized neural area, but emerges out of the interaction of visual information organized by spatial structuring capacities correlated with lower, higher, and intermediate levels of the visual hierarchy. After clarifying different notions of emergence and elaborating evidence for IHS, I discuss how IHS can be tested through transcranial magnetic stimulation and masking. In the final section I present some further implications/advantages of IHS.

Subjective experience has often taken center stage in debates between competing conceptual theories of the mind. This is also a central object of concern in the empirical domain, and especially in the search for the neural correlates of consciousness (NCCs). By now, most of the competing conceptual theories of consciousness have become aligned with distinct hypotheses about the NCCs. These hypotheses are usually distinguished by reference to their proposed location of the NCCs. This difference in hypothesized location of the NCCs has tempted participants in these debates to infer that evidence indicating the location of the NCCs in one or the other brain region can be taken as direct evidence for or against a given conceptual theory of consciousness. We argue that this is an overestimation of the work finding the NCCs can do for us, and that there are principled reasons to resist this kind of inference. To show this we point out the lack of both an isomorphism and a homomorphism between the conceptual frameworks in which most theories are cached, and the kind of data we can get from neuroimaging. The upshot is that neural activation profiles are insufficient to distinguish between competing theories in the conceptual domain. We suggest two ways to go about ameliorating this issue.

Despite that leading theories of consciousness make diverging predictions for where and how neural activity gives rise to subjective experience, they all seem to partially agree that the neural correlates of consciousness (NCC) require globally integrated brain activity across a network of functionally specialized modules. However, it is not clear yet whether such functional configurations would be able to identify the NCC. We scanned resting-state fMRI data from 21 subjects during wakefulness, propofol-induced sedation, and anesthesia. Graph-theoretical analyses were conducted on awake fMRI data to search for the NCC candidates as brain regions that exhibit both high rich-clubness and high modular variability, which were found to locate in prefrontal and temporoparietal cortices. Another independent data set of 10 highly-sampled subjects was used to validate the NCC distribution at the individual level. Brain module-based dynamic analysis revealed two discrete reoccurring brain states, one of which was dominated by the NCC candidates (state 1), while the other state was predominately composed of primary sensory/motor regions (state 2). Moreover, state 1 appeared to be temporally more stable than state 2, suggesting that the identified NCC members could sustain conscious content as metastable network representations. Finally, we showed that the identified NCC was modulated in terms of functional connectedness and modular variability in response to the loss of consciousness induced by propofol anesthesia. This work offers a framework to search for neural correlates of consciousness by charting the brain network topology and provides new insights into understanding the roles of different regions in underpinning human consciousness.

Researchers on the neural correlates of consciousness (NCC) need to distinguish mere statistical NCCs from NCCs proper. Some neural events may be co-occurrent, probabilistically coupled, or coincidental with a type of conscious experience but lack any deeper connection to it, while in other cases, the relation between neural states and a type of experience hints at a strong metaphysical relation, which distinguishes such NCCs proper from mere statistical NCCs. In order to address this issue of how to distinguish NCCs proper from mere statistical NCCs, we propose a position we call neurophenomenal structuralism. The position hinges on the uncontroversial idea that phenomenal experiences relate to each other in degrees of similarity and difference. These complex structures are used to identify and individuate experiences in the methods of neuroscience, psychophysics, and phenomenology. Such individuation by structure leads to phenomenal holism, which has implications for how to investigate consciousness neuroscientifically and generates a constraint by which we can distinguish NCCs proper from mere statistical NCCs: the structural similarity constraint. Neural activation must preserve the structure governing the domain of experiences it is associated with in order to count as that domain’s NCC proper. Any activation that fails to preserve phenomenal structure fails to be an NCC proper. We illustrate how this constraint works with a study by Brouwer & Heeger (2009) as an example.

There is an extensive body of literature linking ADHD to overweight and obesity. Research indicates that impulsivity features of ADHD account for a degree of this overlap. The neural and polygenic correlates of this association have not been thoroughly examined. In participants of the IMAGEN study, we found that impulsivity symptoms and body mass index (BMI) were associated (r = 0.10, n = 874, p = 0.014 FWE corrected), as were their respective polygenic risk scores (PRS) (r = 0.17, n = 874, p = 6.5 × 10−6 FWE corrected). We then examined whether the phenotypes of impulsivity and BMI, and the PRS scores of ADHD and BMI, shared common associations with whole-brain grey matter and the Monetary Incentive Delay fMRI task, which associates with reward-related impulsivity. A sparse partial least squared analysis (sPLS) revealed a shared neural substrate that associated with both the phenotypes and PRS scores. In a last step, we conducted a bias corrected bootstrapped mediation analysis with the neural substrate score from the sPLS as the mediator. The ADHD PRS associated with impulsivity symptoms (b = 0.006, 90% CIs = 0.001, 0.019) and BMI (b = 0.009, 90% CIs = 0.001, 0.025) via the neuroimaging substrate. The BMI PRS associated with BMI (b = 0.014, 95% CIs = 0.003, 0.033) and impulsivity symptoms (b = 0.009, 90% CIs = 0.001, 0.025) via the neuroimaging substrate. A common neural substrate may (in part) underpin shared genetic liability for ADHD and BMI and the manifestation of their (observable) phenotypic association.

Multiple Perspectives on Consciousness for Cognitive Science Richard A. Carlson (racarlson@psu.edu) Department of Psychology, Penn State University 613 Moore Building, University Park, PA 16802 USA The huge contemporary literature on consciousness spans multiple disciplines, including psychology, philosophy, and neuroscience. This tutorial will introduce participants to major proposals about consciousness, and their empirical and methodological implications. The goal is to prepare participants to explore the consciousness literature in greater depth. Our consideration of perspectives on consciousness will be organized by considering how these perspectives address core questions about consciousness, including: (a) How can subjectivity and agency be accommodated in a scientific theory of consciousness? (b) How can conscious and nonconscious or unconscious processes and representations be systematically distinguished? (c) How can conscious mental states be assessed or measured? (d) How can dissociations and impairments of consciousness be understood? The literatures to be considered address these questions in analytic, functional, computational, and implementational terms. Philosophical Perspectives Philosophers approach the problem of consciousness from a variety of analytic perspectives, some focusing on contemporary formulations of the mind-body problem and others on analyses of subjective experience. Among the philosophical perspectives we will consider are John Searle’s (1992) analysis of consciousness in terms of intentionality, David Chalmer’s (1996) distinction between “easy” and “hard” problems of consciousness, David Rosenthal’s (1993) “higher order thought” proposal, and Daniel Dennett’s (1991) “multiple drafts” theory of consciousness. Neuroscience Perspectives Neuroscientists have made a wide variety of proposals concerning the neural correlates of consciousness (NCC). A starting assumption is that a subset of current neural activity is correlated with current conscious experience. There is controversy, however, concerning how that subset is to be identified. For example, the NCC might be limited to particular types of cells or anatomical structures, or comprise global patterns of synchronized neural activity. We will consider recent proposals concerning NCC by Crick and Koch (1998), Damasio (2000), and Edelman and Tononi Psychological Perspectives Psychological perspectives on consciousness generally focus on functionally-defined aspects of cognition. For example, psychologists have identified consciousness with working memory (Baars, 1988), attention (Schneider & Pimm-Smith, 1997), metacognition (Nelson, 1996), and with the structure of mental states (Carlson, 1997). Cognitive research often focuses on distinguishing conscious and nonconscious influences on psychological processes such as learning (Dienes & Berry, 1997) and perception (Merikle, Smilek, & Eastwood, 2001). This research has generated a rich literature on methods for assessing consciousness. References Baars, B. J. (1988). A cognitive theory of consciousness. New York: Cambridge University Press. Carlson, R. A. (1997). Experienced Cognition. Mahwah, NJ: Lawrence Erlbaum Associates. Chalmers, D. (1996). The conscious mind. Oxford: Oxford University Press. Crick, F., & Koch, C. (1998). Consciousness and neuroscience. Cerebral Cortex, 8, 97-107. Damasio, A. R. (2000). A neurobiology for consciousness. In T. Metzinger (Ed.), Neural correlates of consciousness Cambridge, MA: The MIT Press. Dienes, Z., & Berry, D. (1997). Implicit learning: Below the subjective threshold. Psychonomic Bulletin and Review, 4, Dennett, D. C. (1991). Consciousness explained. Boston: Little, Brown and Company. Edelman, G. M., & Tononi, G. (2000). Reentry and the dynamic core: Neural correlates of conscious experience. In T. Metzinger (Ed.), Neural correlates of consciousness. Cambridge, MA: The MIT Press. Merikle, P. M., Smilek, D., & Eastwood, J. D. (2001). Perception without awareness: perspectives from cognitive psychology. Cognition, 79, 115-134. Nelson, T. O. (1996). Consciousness and metacognition. American Psychologist, 51, 102-116. Rosenthal, D. M. (1993). Thinking that one thinks. In M. Davies, & G. W. Humphreys (Eds.), Consciousness: Psychological and philosophical essays. Oxford: Blackwell. Searle, J. R. (1992). The rediscovery of the mind. Cambridge, MA: The MIT Press. Schneider, W., & Pimm-Smith, M. (1997). Consciousness as a message aware control mechanism to modulate cognitive processing. J. Cohen, & J. Schooler (Eds.), Scientific approaches to consciousness: The 25th Carnegie Symposium on Cognition. Mahwah, NJ: Erlbaum.

Neurons in Area V4 of the Macaque Translate Attended Visual Features into Behaviorally Relevant Categories

"Paradox of slow frequencies" - Are slow frequencies in upper cortical layers a neural predisposition of the level/state of consciousness (NPC)?

The neurological basis for perceptual awareness remains unclear, and theories disagree as to whether sensory cortices per se generate awareness. Critically, neural activity in the sensory cortices is only a neural correlate of consciousness (NCC) if it closely matches the contents of perceptual awareness. Research in vision and touch suggest that contralateral activity in sensory cortices is an NCC. Similarly, research in hearing with two sound sources (left and right) presented over headphones also suggests that a candidate NCC called the auditory awareness negativity (AAN) matches perceived location of sound. The current study used 13 different sound sources presented over loudspeakers for natural localization cues and measured event-related potentials to a threshold stimulus in a sound localization task. Preregistered Bayesian mixed models provided moderate evidence against an overall AAN and very strong evidence against its lateralization. Because of issues regarding data quantity and quality, exploratory analyses with aggregated data from multiple loudspeakers were conducted. Results provided moderate evidence for an overall AAN and strong evidence against its lateralization. Nonetheless, the interpretations of these results remain inconclusive. Therefore, future research should reduce the number of conditions and/or test over several sessions to procure a sufficient amount of data. Taken at face value, the results may suggest issues with AAN as an NCC of auditory awareness, as it does not laterally map onto experiences in a free-field auditory environment, in contrast to the NCCs of vision and touch.

The authors are right in holding the viewthat neural synchrony does not seem toprovide a solution for the ‘hard problem ofconsciousness’ (Chalmers 1996). They arealso right in that most of the evidencepresented for the role of neuralsynchronization in perceptual binding iscorrelative and not causal. They areessentially wrong in all their remainingpoints.It is true that neural synchrony does notsolve the hard problem, but then, nobodyhas proposed a solution for the hardproblem. It is not even clear that such aproblem exists or that a scientific solutioncan ever be given to the hard problem(Dennett 1991). Certainly it is premature tomake a definitive statement on this subjectat the present stage of research.By contrast, neural synchrony does seemto be at least part of the neural correlates ofconsciousness, which ask what are theminimal neural activities and structures thatare necessary and sufficient for a consciousact to take place (Crick & Koch, 1990). In arecent paper we have been able to showthat, long-range synchrony correlates withvisual awareness but local synchrony doesnot (Melloni et al. 2007). This result,suggests that synchronic activity inside arestricted cortical area remains unconsciousand that consciousness arises only when ‘allthe brain’ is informed via long-rangesynchronic interactions. It can behypothesized that this would be the basisfor the unified character of experientialconsciousness.The authors correctly point to thecorrelative nature of most of the evidencesupporting a role of neural synchrony bothin consciousness and in visual featurebinding. To our knowledge there is a singleexperiment showing the causal involvementof neural synchrony in an odordiscrimination task (Stopfer et al. 1997).However it must be stated that the sameholds true for all electrophysiology in allthe fields of neuroscience. From the studiesof Hubel and Wiesel on, essentially allelectrophysiology consists of manipulatingthe stimuli, recording the neural responseand proposing mechanisms based on thecorrelations found. The only alternativetheory for visual binding (the cardinal celltheory, Barlow 1972) is also mostly basedon correlative evidence with the onlyexception of a few works conducted byShadlen and collaborators (Huk & Shadlen2005)An argument is made against synchronyas a mechanism for consciousness becauseof the participation of synchrony in non-conscious (anesthetized) animals and inbrain areas not obviously related toperceptual consciousness (thehippocampus). Both arguments arelogically false. The fallacy is tantamount toclaiming that because

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