Bistability of prefrontal states gates access to consciousness

Abstract

In perceptual multistability, the content of consciousness alternates spontaneously between different interpretations of unchanged sensory input. The source of these internally driven transitions in conscious perception is unknown. Here we show that transient, low frequency (1-9 Hz) perisynaptic bursts in the macaque lateral prefrontal cortex precede spontaneous perceptual transitions in a no-report binocular motion rivalry task. These lowfrequency transients suppress 20-40 Hz oscillatory bursts that selectively synchronise the discharge activity of neuronal ensembles signalling conscious content. Similar ongoing state changes, with dynamics resembling the temporal structure of spontaneous perceptual alternations during rivalry, dominate the prefrontal cortex during resting-state, thus pointing to their default, endogenous nature. Our results suggest that prefrontal state fluctuations control access to consciousness through a reorganisation in the activity of feature-specific neuronal ensembles. One sentence summaryPrefrontal state transitions precede spontaneous transitions in the content of consciousness. | Pageusing a no-report BR paradigm. This allowed us to detect intrinsically driven transitions in conscious perception of opposing directions-of-motion. We combined this task with multielectrode recordings of local field potentials (LFPs) and simultaneously sampled direction-of-motion selective, competing ensembles. By using the optokinetic nystagmus (OKN) reflex as an objective criterion of perceptual state transitions, we removed any effects of voluntary motor reports on neural activity, identifying signals directly related to spontaneous transitions in the content of consciousness. ResultsWe used a no-report paradigm of binocular motion rivalry coupled with multielectrode extracellular recordings of LFPs and direction-of-motion selective neuronal ensembles in the inferior convexity of the macaque PFC ( Fig. 1A). Two types of trials were employed: a) physical alternation (PA) of monocular alternating, opposing directions of motion and b) binocular rivalry (BR) where the initial direction of motion was not removed but was followed by a flashed, opposing direction of motion in the contralateral eye ( Fig. 1B, upper panel).Initially, this manipulation results in an externally induced period of perceptual suppression of variable duration for the first stimulus (binocular flash suppression -BFS) which is followed by spontaneous perceptual transitions since the two competing representations start to rival for access to consciousness. In order to exclude the effect of voluntary perceptual reports on neural activity the macaques were not trained to report their percept. Instead, the polarity of their motion-induced optokinetic nystagmus reflex (OKN) elicited during passive observation of the stimuli (in both conditions, i.e. BR and PA), and previously shown to provide an accurate perceptual state read-out in both humans and macaques, was used to infer perceptual dominance periods (Fig. 1B, lower panel). These domin...

Evidence for an Active Role of Inferior Frontal Cortex in Conscious Experience

“…With respect to the role of prefrontal cortex in consciousness, our results clearly speak against the notion that IFC activates merely as a consequence of perceptual events that are generated within sensory cortices 26–28 . In line with recent electrophysiological data in monkeys 54 , our findings strengthen existing theoretical accounts 6,8–10 that assume a critical role of prefrontal cortex in consciousness. As a significant extension, our work associates IFC with a specific computational function for conscious experience: In iterative feedback- and feedforward-interactions with sensory brain regions, IFC may determine how swiftly conscious experience is updated in response to perceptual conflict 19,20,23 .…”

Fluctuations of consciousness, mood, and science: The interhemispheric switch and sticky switch models two decades on

“…Most recently, Abhilash Dwarakanath, Vishal Kapoor, Nikos Logothetis, Theofanis Panagiotarapoulos and colleagues (Dwarakanath et al, 2020) reported striking new electrophysiological findings obtained during BR in alert macaque monkeys during a no‐report protocol. These findings are highly relevant to the work Pettigrew and I started.…”

“…Most of our work is consistent with the former, referring as we did to pacemaker neurons, clocks, and genetic period‐coupling of BR to ultradian and other biological rhythms (Pettigrew & Miller, 1998; Pettigrew, 2001; Pettigrew & Carter, 2005; Miller et al, 2012). The new data from Dwarakanath et al (2020) speak directly to the question of whether the BR oscillator is endogenous.…”

“…Dwarakanath et al (2020) found LFP recordings revealed that transient low frequency (1–9Hz) perisynaptic bursts in lateral prefrontal cortex precede spontaneous perceptual switches during BR and that these transients suppress oscillatory bursts in the beta (20–40Hz) range. The latter selectively synchronize discharge activity of feature‐specific neural ensembles that signal conscious content, so their suppression by the low frequency transients potentially allows for increasing neural spiking in the suppressed population, thus increasing the likelihood of perceptual reorganization.…”

Uncovering the Organization of Neural Circuits with Generalized Phase Locking Analysis

“…Understanding brain function requires uncovering the relationships between neural mechanisms at different scales (Einevoll et al, 2019): from single neurons to microcircuits (Rasch et al, 2008, Voytek, 2018 and various cognitive functions, such as perceptual binding (Engel et al, 1999), visual awareness (Dwarakanath et al, 2020), attention (Niebur et al, 1993) and memory (Buzsaki, 2006). These oscillations manifest themselves in Local Field Potentials (LFP), a mesoscopic extracellular signal (Liljenstroem, 2012) resulting from ionic currents flowing across the cellular membranes surrounding the electrode.…”