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A , Depiction of the problem. We aim for the correlation between a conscious content and a given brain state. What is measured experimentally is the correlation between a behavioral report and a measure of brain activity, which might be appropriate or not. Report-related neural activity poses a confound for the NCC. B , Involuntary physiological measures taken to infer the perceptual state of a subject to circumvent the behavioral report Tononi et al.

Human patients and monkeys with lesions in primary visual cortex V1 are blind at the corresponding visual field location; therefore, the role of V1 as a prerequisite for visual consciousness seems unequivocal Tong, ; Maier et al.

2.1 What is Consciousness Part I

On the other hand, the causal contribution of neural populations in area V1 or LGN as a possible substrate of conscious perception is difficult to evaluate in lesion studies because they also constitute prerequisites that might be subtracted out in the typical contrastive approach. Indeed, using a spatial decision paradigm with directed eye movements versus button presses showed that inferior parietal lesions in humans interfere with directed saccade choices but not with visual perception reported with button presses Ro et al. A , Major cortical and subcortical brain regions where lesions lead to spatial neglect in humans left , and corresponding recent experimental results in monkeys right lateral view.

In humans, lesions in frontal Brodmann area 44 , inferior parietal cortex Brodmann area 40 , superior temporal gyrus STG , basal ganglia, and pulvinar have been reported to lead to spatially biased behavior that might appear as a visual consciousness deficit Karnath, B , Recent pharmacological inactivation studies in monkeys have shown primarily effector-specific spatial deficits after lesions in parietal subregions such as the lateral intraparietal area LIP, red shading and the parietal reach region PRR, which includes the medial intraparietal area MIP and area V6A, green shading.

Dorsal pulvinar dPULV, orange shading inactivation leads to spatial orienting bias for both eye and hand movements which can be compensated by visual reward cues, suggesting that visual perception might be preserved. Ventral pulvinar vPULV, purple shading inactivation leads to change detection deficits resembling visual neglect.

Summarized from local inactivation studies in monkeys Wardak et al. A similar case can be made for the dorsal pulvinar, which strongly interconnects with frontoparietal cortices. Spiking rates of pulvinar neurons in monkeys strongly correlate with reported perception Wilke et al. However, pulvinar as well as parietal cortices might contain subregions that are more closely related to visual consciousness as opposed to visuomotor behavior Driver and Mattingley, ; Ward et al.

Thus, deciphering regional specificity and the further development and application of behavioral paradigms that allow the distinction between perceptual and action planning deficits will remain important. From the beginnings of NCC studies, it has been widely assumed that the prefrontal cortex plays a critical role in enabling both contents and levels of consciousness Crick and Koch, ; Leopold and Logothetis, ; Cruse et al. Because the role of the prefrontal cortex has recently emerged as one of the most controversial issues in NCC research Pennartz, ; Koch et al.

It has been widely assumed that prefrontal cortex is critical for consciousness as part of a frontoparietal network Del Cul et al. However, recent evidence from lesion, stimulation, and neuroimaging studies challenges this assumption.

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Lesion studies have provided several reports of patients with a normal level of consciousness after extensive frontal damage. By contrast, traumatic lesions of the posterior corpus callosum, connecting large parts of the posterior cortex, carry a fold increased risk of permanent vegetative state Kampfl et al.

With regard to the contents of consciousness, there is no clear evidence for loss of specific experiential contents after frontal damage Penfield and Jasper, Similarly, while lesions in frontal cortices have been reported to lead to overt visually guided orienting deficits, they hardly lead to impairments of conscious contents per se Na et al. In contrast, abundant neurological evidence points to lesions in the posterior cortex causing a loss of specific contents of experience Farah, For example, lesions of the right fusiform face area may cause unconsciousness of faces, and lesions of inferolateral occipital cortex unconsciousness of colors Barton, Electrical stimulation of most of the frontal cortex fails to elicit content-specific changes in experience Penfield and Jasper, , although it can induce involuntary movements or interfere with task performance Selimbeyoglu and Parvizi, In contrast, electrical stimulation of posterior cortex more reliably induces discrete changes in conscious contents.

For example, direct electrical stimulation of early visual areas induces phosphenes Beauchamp et al. Compared with lesion and stimulation studies, neuroimaging studies offer less direct evidence for the contribution of any one brain region to consciousness Farah, However, neuroimaging experiments can demonstrate dissociations between the NCC and those of other cognitive processes Aru et al.

While studies comparing vegetative state patients to healthy volunteers highlighted differences in both frontal and parietal cortices and in thalamocortical connectivity Gosseries et al. In awake volunteers, studies using stimuli that are task irrelevant but experienced thereby dissociating consciousness from cognitive functions involved in task demands; Aru et al. In contrast, content-specific NCC at frontal recording sites P3 component was only found when the stimuli were task-relevant.

The advent of large-scale neuroimaging databases can now help to quantify systematic associations between specific conscious contents and the activation of specific cortical areas by using meta-analytic reverse inference Poldrack, ; Yarkoni et al. In agreement with lesion and stimulation studies, reverse inference analyses performed, for example, with Neurosynth www. In all these cases, reverse inference fails to highlight frontal areas as predictive for the presence of specific contents of consciousness Boly et al.

Multivariate decoding techniques can also help to identify the true NCC as the brain activity patterns that have the highest predictive value for specific conscious percepts Haynes, ; Sandberg et al. Using such approaches, the best predictor for the presence versus absence of consciousness has been located in temporo-parieto-occipital cortices both during non-rapid eye movement NREM sleep Siclari et al. While studies comparing brain function during anesthesia versus wakefulness consistently highlighted differences in both frontal and parietal cortices and in thalamocortical connectivity Alkire et al.

On the other hand, the predictive value of posterior cortex activity for consciousness during anesthesia still needs to be assessed Boly et al. With regard to the contents of consciousness, numerous studies in both awake and dreaming subjects could decode the presence of specific conscious contents from specific activity patterns in posterior cortex Nishimoto et al. Working memory contents can also be more reliably decoded from the back than from the front of the cortex Emrich et al. By contrast, evidence for a content-specific contribution of the prefrontal cortex is scarce or indirect.

At a minimum, detailed descriptions of conscious patients after extensive bilateral frontal resections demonstrate that an entirely intact prefrontal cortex is not necessary for consciousness. It remains possible that some prefrontal regions may contribute specific conscious contents, such as feelings of reflection, valuation, and affect Koch et al. In the future, within-state paradigms applied to sleep dreaming Siclari et al. Detecting the presence of consciousness in clinical practice relies ultimately on a behavioral input—output paradigm: a neurologist typically probes the patient with sensory stimuli of different modalities or verbal commands and observes his motor responses Giacino et al.

If the patient reliably produces outputs that are specific for the different inputs, he is considered conscious. The earlier sections of this review already pointed out that this approach can be problematic: unresponsiveness can be paired with consciousness. However, thanks to recent conceptual and technical advances, a similar input—output paradigm can now be applied even to patients who are fully paralyzed and cannot engage in motor behavior Owen et al. In this case, subjects are still presented with sensory stimuli or verbal instructions e.

Frontiers | The Confluence of Perceiving and Thinking in Consciousness Phenomenology | Psychology

These neuroimaging paradigms can be easily interpreted in case of positive results: unresponsive subjects who willfully produce neuronal activations that are consistent and specific for the given input are considered conscious. However, many brain-injured patients may recover consciousness, yet fail to produce the appropriate neuronal responses Monti et al.

For example, during dreaming, complex, temporally unfolding episodes can be as intense and vivid as waking experiences, yet sensory stimuli are typically ignored and rarely incorporated into the experience Koulack, ; Nir and Tononi, Consciousness may completely disconnect from the external environment also during some forms of anesthesia, such as ketamine, which induces a dreamlike, hallucinatory state associated with sensory disconnection and complete unresponsiveness Hejja and Galloon, Similar disconnections may occur in pathological conditions, whereby patients may be conscious but fail to produce the right neuronal responses to peripheral stimuli just because their sensory pathways and cortices are damaged or functionally disabled.

Indeed, intensive care medicine is artificially producing, as a byproduct of saving many lives, brains that may remain isolated, split, or fragmented Schiff et al. In the extreme case, large cortical islands, or an archipelago of islands, may survive totally dissociated from the world outside Gosseries et al. Can these islands sustain consciousness? Does it feel like anything to be a big chunk of isolated human cortex?

For now, we cannot answer this question. To address this problem, it would be useful to develop complementary metrics to probe directly the internal brain capacity for consciousness i. Thus, PCI gauges directly the amount of information differentiation that can be generated through large-scale causal interactions integration within the thalamocortical system. Operationally, the index quantifies the complexity algorithmic compressibility of the EEG response to a direct cortical perturbation with TMS. The EEG echo will be both global and differentiated i.

Brain complexity was lower in all unresponsive subjects who did not report any conscious experience upon awakening from NREM sleep or midazolam, xenon, and propofol anesthesia, and was invariably higher in conditions in which consciousness was present, including awake controls and subjects who were disconnected and unresponsive during rapid eye movement REM sleep and ketamine anesthesia but retrospectively reported having had vivid conscious experiences upon awakening. In these behaviorally unresponsive patients, PCI values overlapped with the distribution of the benchmark conscious condition, suggesting the presence of disconnected consciousness, which eventually resulted in a higher rate of recovery Casarotto et al.

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  7. Measuring complexity and studying its mechanisms in the brain may also offer valuable insights on the neuronal bases of loss and recovery of consciousness. TMS is a strong, coarse-grained perturbation that activates many diverging cortical and corticosubcortical connections; therefore, PCI is a global measure that cannot resolve whether there are preferential hubs of complexity within the brain e.

    Ongoing studies using localized, intracortical single-pulse electrical stimuli and mesoscale local field potential recordings may provide deeper insight. For example, a recent intracranial human study Pigorini et al. Second, they can be investigated from the intracellular level in animal models Steriade et al. Third, they can impair network interactions globally Lewis et al. Notably, a recent microscale study using electrical stimulation and recordings in isolated cortical slices an extreme case of cortical island showed that complex causal interactions, as assessed by an adapted version of PCI, can be restored by pharmacological manipulations that reduce neuronal bistability D'Andola et al.

    Can some of these concepts be translated to the bedside of comatose patients?

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    Will we be able to understand and promote this process? In the years to come, it will be crucial to further elucidate the relationships between single-neuron dynamics, overall network complexity, and consciousness through extensive experiments across scales, species, and models. Animal models provide a unique window to probe the neuron-level mechanisms of many cognitive processes, including consciousness.

    Rodents, in particular, offer an unprecedented range of tools to access all circuital elements of the brain, and share many features with the human brain. However, when addressing the question of consciousness in rodents or other animals, it is crucial to ask whether these animals can be conscious at all.

    It is a valid question regardless of species, applying to nonhuman primates as well as rodents. The question of rodent consciousness can be split into two components: 1 do rodent brains have conscious states as opposed to unconscious states e. The first question is less difficult to address than the second, as is also the case for nonhuman primates and humans: conscious contents refer to subjective and qualitative aspects of our experiences, which are notoriously hard to get at due to their essentially private nature.

    In contrast, there are several arguments in favor of rodents having at least a basic capacity to sustain conscious states: 1 the fact that electrophysiological markers indicative of conscious states in humans and primates are also found in rodent brains e. Such indicators do not only include sleep—wake cycles and markers of wakefulness, such as behavioral reactivity to sensory stimuli and orienting responses, but also the ability to generate nonhabitual i.

    A fourth argument is based on recently developed measures of consciousness Massimini et al. As in humans and primates, wakeful states in rodents are marked by a higher degree of complexity Hudetz et al. While many questions also regarding this argument remain open in rodents, our best, evidence-based guess is that rodent brains are indeed capable of sustaining conscious states, regardless of the precise complexity and richness of represented contents compared with primates.

    Here we will review recent findings related to this fourth argument, and discuss how they expand our understanding of NCCs in the rodent brain. The ability to integrate complex information and generate interactions sustaining world representations eventually resides in the brain's information-coding elements: neurons. Because most previous comparisons between conscious, sleep, and anesthetized states in humans have used recording techniques with macroscopic and mesoscopic resolution Massimini et al.

    The few studies on the topic are somewhat inconsistent and report either no change in functional connectivity between conscious and unconscious states Zhang et al. We investigated this using multiarea tetrode recordings in sensory neocortex and hippocampus of rats undergoing transitions from wakefulness to NREM sleep for methods, see Bos et al.

    Reflections and Meditations, episode 5: The Mind and the Brain (Bernardo Kastrup)

    We computed conditional mutual information cMI to quantify functional connectivity between spike train patterns across all cell pairs, as this measure includes nonlinear correlations that would escape detection by linear methods Steuer et al. Although the results showed area-specific changes in correlation patterns, they confirmed that global functional connectivity drops from wakefulness to NREM sleep Olcese et al. This effect was due to a selective loss of interareal interactions between excitatory neurons but not interneurons, whereas intra-areal connectivity was largely preserved for both neuronal types Fig.

    Because cMI does not indicate the direction of information flow between neurons, we also computed the transfer entropy between spiking neurons, and found that this measure allows to distinguish several regimes for directed communication in the brain, depending on the time scale of neural interaction, the anatomical distance between neurons, and, intriguingly, the presence of a neural correlate to the behavioral task performed by the animal before NREM sleep U.

    A , Summary of main findings on spike-based functional connectivity in rats Olcese et al. Coupling was measured as pairwise cMI between single neurons.

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    8. During wakefulness, cMI between neurons located in the same or different areas is largely balanced left for both excitatory and inhibitory neurons black and red lines, respectively.