Global workspace dynamics: cortical "binding and propagation" enables conscious contents

Abstract

A global workspace (GW) is a functional hub of binding and propagation in a population of loosely coupled signaling elements. In computational applications, GW architectures recruit many distributed, specialized agents to cooperate in resolving focal ambiguities. In the brain, conscious experiences may reflect a GW function. For animals, the natural world is full of unpredictable dangers and opportunities, suggesting a general adaptive pressure for brains to resolve focal ambiguities quickly and accurately. GW theory aims to understand the differences between conscious and unconscious brain events. In humans and related species the cortico-thalamic (C-T) core is believed to underlie conscious aspects of perception, thinking, learning, feelings of knowing (FOK), felt emotions, visual imagery, working memory, and executive control. Alternative theoretical perspectives are also discussed. The C-T core has many anatomical hubs, but conscious percepts are unitary and internally consistent at any given moment. Over time, conscious contents constitute a very large, open set. This suggests that a brain-based GW capacity cannot be localized in a single anatomical hub. Rather, it should be sought in a functional hub - a dynamic capacity for binding and propagation of neural signals over multiple task-related networks, a kind of neuronal cloud computing. In this view, conscious contents can arise in any region of the C-T core when multiple input streams settle on a winner-take-all equilibrium. The resulting conscious gestalt may ignite an any-to-many broadcast, lasting ∼100-200 ms, and trigger widespread adaptation in previously established networks. To account for the great range of conscious contents over time, the theory suggests an open repertoire of binding coalitions that can broadcast via theta/gamma or alpha/gamma phase coupling, like radio channels competing for a narrow frequency band. Conscious moments are thought to hold only 1-4 unrelated items; this small focal capacity may be the biological price to pay for global access. Visuotopic maps in cortex specialize in features like color, retinal size, motion, object identity, and egocentric/allocentric framing, so that a binding coalition for the sight of a rolling billiard ball in nearby space may resonate among activity maps of LGN, V1-V4, MT, IT, as well as the dorsal stream. Spatiotopic activity maps can bind into coherent gestalts using adaptive resonance (reentry). Single neurons can join a dominant coalition by phase tuning to regional oscillations in the 4-12 Hz range. Sensory percepts may bind and broadcast from posterior cortex, while non-sensory FOKs may involve prefrontal and frontotemporal areas. The anatomy and physiology of the hippocampal complex suggest a GW architecture as well. In the intact brain the hippocampal complex may support conscious event organization as well as episodic memory storage.

Keywords: attention; awareness; brain dynamics; consciousness; cortex; global workspace theory; theoretical biology; voluntary control.

Figure 1

Binding and broadcasting from many locations. Four alternative sources of binding and broadcasting in the C-T core. Sites of possible binding and broadcasting are shown as yellow starbursts. Because global broadcasts mutually interfere, only one can occur in any 100–200 ms period. Global interference may explain the limited capacity of momentary conscious contents. Areas V1 and IT: visuotopic maps include area V1, the first cortical map for vision, and area IT, where conscious object representations emerge (Logothetis, 1998). Different coalitions of anatomically identical spatiotopic activity maps may lead to different conscious experiences, like the sight of a single star on a dark night (V1) vs. a coffee cup within arm’s reach (IT). Prefrontal cortex: non-sensory “feelings of knowing” may bind and broadcast from non-sensory cortex. Area MTL: we predict that the intact medial temporal cortex contributes to subjective event organization as well as episodic memory coding (See The Hippocampus and Conscious Contents: a Novel Prediction).

Figure 2

Feature binding by adaptive resonance. Darwin VII’s biologically based visuotopic arrays employ adaptive resonance (reentry) to transform optical input into neuron-like activation patterns. Darwin VII was able to bind visual features given the known connectivity of visual cortical areas V1, V2, V4, and IT. Some stimuli have positive or negative “value” (incentives). The robot has goals and movement controls, and perceives obstacles. Thus, the robot’s environment helps to constrain its behavior using goals, rewards, obstacles, and the like.

Figure 3

Conscious contents enable access to cognitive functions, including sense modalities, working memory, long term memories, executive decisions and action control. Executive regions of the frontoparietal cortex gain control over distributed unconscious functions via conscious feedback. (Cerf et al., ; Shanahan, 2010).

Figure 4

The C-T complex supports any-to-any signaling. The cortico-thalamic system allows any spatiotopic activity (SA) array to signal any other. Combined with adaptive resonance, this allows an open set of cortical and thalamic coalitions to bind and broadcast information from any region to any other. The left half represents the left hemisphere of the brain, whereas the right half represents the right hemisphere. The brain stem is shown at the bottom. Circular color bars at the bottom describe the scale of the corresponding anatomical ring.

Figure 5

Any-to-many signaling in conscious vision. While the structure of the cortico-thalamic system suggests any-to-any signaling, effective (causal) connectivity requires measures of signal traffic flow rather than structural connectivity. Doesburg et al. (2008) were able to show “any-to-many” signaling using simple LED stimuli in the lateral periphery of each hemifield. The figure shows a left-lateralized light stimulus triggering a broadcast from early right visual cortex.

Figure 6

Long-distance phase-locking in the waking state. The waking state shows hidden regularities. During waking, intracranial EEG shows phase-locking between different parts of cortex, and between the hippocampus and neocortex. While the overall sound of the waking stadium may seem random, local conversations can show precise phase coupling. Notice that deep sleep and dreaming show almost no phase coupling between distant cortical regions, or between cortex and hippocampus.

Figure 7

Intracranial recordings in epileptic patients have 1,000 times the signal-to-noise ration of scalp recordings, and therefore reveal much more detail. Crone et al. (2006) published these images of the left lateral hemisphere in a conscious epileptic patient before surgery, listening to a spoken word (A) and speaking it (B). Conscious patients in this procedure experience little pain under local anesthetic. White numbered disks are electrodes, and purple arrows between them indicate event-related synchrony (ERS) as shown in the graphs. In Task (A) “Hearing a word,” ERS bursts in four gamma bands occur 100–600 ms post stimulus. In Task (B) “Speaking a word” ERS gamma starts before the response, and continue during the next two seconds in 100–200 ms bursts. Task (A) shows widespread left hemisphere ERS, while in Task (B) is ERS is localized near Broca’s area for speech production. Other studies show precise ERS bursts in cortex for sensory processing, response organization and memory coding. Cortical synchrony may be a task-specific signaling code.

Figure 8

VAN: the visual awareness negativity wave. The small conscious content-linked component of the visual awareness ERP (VAN) appears about 300 ms after a visual stimulus and lasts for 1–200 ms. It appears to sweep forward, and may be followed by a late positivity (LP). The VAN has been observed in more than a dozen studies comparing conscious to unconscious visual stimuli that are identical at the retina.

Figure 9

EEG microstates at theta rates in humans and rabbits. Global microstates have been found using several methods. Freeman et al. (2003) used Hilbert analysis to observe fast phase changes at theta rates in entire cortical hemispheres in humans and rabbits. The vertical axis shows phase differences in radians, revealing stable states for 100–200 ms, interrupted by a hemisphere-wide near–instantaneous collapse for 5–10 ms before a new equilibrium is achieved. The horizontal axes show time (in ms) and electrodes.

Figure 10

Perceptual experiences vs. feelings of knowing (FOKs). This dGW cartoon shows an occipital broadcast (which must mobilize parietal egocentric and allocentric maps as well) evoking spatiotopic activity in the prefrontal cortex, which is known to initiate voluntary actions (see yellow arrow). Prefrontal activity is shown as a second global workspace burst, consistent with Figure 1. Visuotopic coding is preserved in the dorsolateral prefrontal cortex. The ability to voluntarily report or act upon a spatially specified stimulus follows from this double binding and broadcasting event. Thus, a posterofrontal broadcast is quickly followed by a centrifugal burst from prefrontal regions, including supplementary motor, premotor, and motor cortex. Posterior binding and broadcasting is experienced as a visual event framed in nearby space, while the prefrontal broadcast is a feeling of knowing (FOK) or “fringe” experience (James, 1890).

Figure 11

Cortical adaptation as a novel task becomes automatic. Schneider (2009) summarized a large literature on habituation of over learned skills. On the left, high BOLD activations are shown in the cognitive control system of the cortex, including the posterior parietal cortex and executive regions of the prefrontal cortex. After the task is practiced to the point of automaticity, only the auditory region of the temporal cortex shows fMRI activity, as required for the auditory detection task. The BOLD signal corresponds to neuronal population activities. These results are consistent with dynamic Global Workspace theory in that the novelty stage involves more conscious and voluntary processing.

Figure 12

Hippocampal-neocortical binding and broadcasting. The hippocampal complex in relation to the neocortex. Notice that the flow of information streams in both directions, with the interesting exception of the subiculum. Thus resonant adaptation can take place in almost all regions of the hippocampal-neocortical complex. This region appears as a major convergence and broadcasting zone, and has been proposed to combine the dorsal and ventral streams of visual cortex (Shimamura, 2010). Direct MTL neuronal recording shows responding to conscious, but not unconscious visual input. Phylogenetically, the hippocampus is ancestral to the neocortex, and controls a fully autonomous sensorimotor brain.