A Synergistic Workspace for Human Consciousness Revealed by Integrated Information Decomposition

Abstract

A central goal of neuroscience is to understand how the brain synthesises information from multiple inputs to give rise to a unified conscious experience. This process is widely believed to require integration of information. Here, we combine information theory and network science to address two fundamental questions: how is the human information-processing architecture functionally organised? And how does this organisation support human consciousness? To address these questions, we leverage the mathematical framework of Integrated Information Decomposition to delineate a cognitive architecture wherein specialised modules interact with a “synergistic global workspace,” comprising functionally distinct gateways and broadcasters. Gateway regions gather information from the specialised modules for processing in the synergistic workspace, whose contents are then further integrated to later be made widely available by broadcasters. Through data-driven analysis of resting-state functional MRI, we reveal that gateway regions correspond to the brain’s well-known default mode network, whereas broadcasters of information coincide with the executive control network. Demonstrating that this synergistic workspace supports human consciousness, we further apply Integrated Information Decomposition to BOLD signals to compute integrated information across the brain. By comparing changes due to propofol anaesthesia and severe brain injury, we demonstrate that most changes in integrated information happen within the synergistic workspace. Furthermore, it was found that loss of consciousness corresponds to reduced integrated information between gateway, but not broadcaster, regions of the synergistic workspace. Thus, loss of consciousness may coincide with breakdown of information integration by this synergistic workspace of the human brain. Together, these findings demonstrate that refining our understanding of information-processing in the human brain through Integrated Information Decomposition can provide powerful insights into the human neurocognitive architecture, and its role in supporting consciousness.

Paths to Oblivion: Common Neural Mechanisms of Anaesthesia and Disorders of Consciousness

“…Future research may build on this finding of regional specificity by seeking to identify whether GABA-A receptor density at specific regions plays an especially prominent role in propofol-induced anaesthesia, or whether concerted action across the entire cortex is required. The prominent involvement of the brain’s default mode network in anaesthesia induced with the GABA-ergic agents propofol and sevoflurane 13,39,40,93,97,98 and more specifically the precuneus/posterior cingulate cortices, suggests that GABA receptor density at these regions may be an especially promising candidate for predicting anaesthetic effects.…”

“…We also studied the fMRI dynamics of a cohort (N=21) of patients suffering from chronic disorders of consciousness (DOC) as a result of severe brain injury (traumatic or anoxic), comparing them with a group of N=20 healthy controls. By subjecting the models to "virtual anaesthesia" (local modulation of inhibitory gain based on empirical GABA-A receptor distribution) and "virtual DOC" (alteration of the model's structural connectome), we sought to identify the neurobiological mechanisms underlying a fundamental question of modern neuroscience: how can transient perturbations of neurotransmission and chronic lesions to the structural connectome, both give rise to unconsciousness and its characteristic similar brain dynamics 13,38,39,41,93 ? Based on a cortical parcellation with 68 regions of interest, each node (cortical region) is modelled through a neurophysiologically realistic biophysical model incorporating excitatory (NMDA) as well as inhibitory (GABA) synaptic dynamics.…”

“…Indeed, our results further indicate that propofol anaesthesia is crucially dependent on the specific regional distribution of GABA-A receptors across the cortex, since neither reshuffling this distribution across regions nor setting all regions to equal density values could reproduce the same effect. Future research may build on this finding of regional specificity by seeking to identify whether GABA-A receptor density at specific regions plays an especially prominent role in propofol-induced anaesthesia, or whether39,40,93,97,98 and more specifically the precuneus/posterior cingulate cortices, suggests that GABA receptor density at these regions may be an especially promising candidate for predicting anaesthetic effects.Remarkably, our PET-informed results showed that considering GABA-mediated scaling of regional inhibitory gain also improved the model's ability to simulate the characteristic dynamics of DOC patients' brains, even though these patients owe their chronic condition to severe brain injury rather than pharmacological intervention. This observation suggests a change of excitatory-inhibitory balance in favour of inhibition, not just in the generation of dynamics pertaining to propofol anaesthesia, but more broadly as a general neurobiological…”

What it is like to be a bit: An Integrated Information Decomposition account of emergent mental phenomena

“…Thus, the information decomposition of Φ provided by ΦID can successfully identify the source of Φ's theoretical difficulties, and provide a straightforward solution. In addition to the theoretical improvement (which will be further discussed below, in the section "A tale of ice and ΦR: From neural dynamics to the ΦR-ing rate"), there is also recent evidence that ΦR also provides empirical advantages over the original formulation of Φ: unlike Φ, ΦR is reduced between the same sets of brain regions both in patients with chronic disorders of consciousness, and during loss of consciousness induced by the intravenous anaesthetic, propofol (Luppi et al, 2020b). Importantly, reductions in ΦR were reversed when participants recovered consciousness after anaesthesia, demonstrating the relevance of ΦR for supporting human consciousness.…”

The Inert Brain: Explaining Neural Inertia as Post-anaesthetic Sleep Inertia

“…This suggests that sleep inertia, at least in the human brain, may correspond to a carry-over of diminished DMN-FPN/DAN anticorrelations. Remarkably, perturbed DMN-FPN/DAN interactions are also one of the most robustly observed neural markers of human loss of consciousness induced by a variety of anaesthetics ( Boveroux et al, 2010 ; Guldenmund et al, 2013 ; Golkowski et al, 2019 ; Luppi et al, 2019 , 2020 ; Huang et al, 2020 ) ( Figure 4 ), and the anticorrelations are even diminished one hour after emergence from sevoflurane anaesthesia ( Nir et al, 2020 ). Thus, we propose that neural inertia may be the effect of anaesthetic-induced sleep inertia, which corresponds to a carry-over of diminished anticorrelations between DMN and FPN/DAN.…”