The Criticality of Consciousness: Excitatory–Inhibitory Balance and Dual Memory Systems in Active Inference

The organization of consciousness is described through increasingly rich theoretical models. We review evidence that working memory capacity—essential to generating consciousness in the cerebral cortex—is supported by dual limbic memory systems. These dorsal (Papez) and ventral (Yakovlev) limbic networks provide the basis for mnemonic processing and prediction in the dorsal and ventral divisions of the human neocortex. Empirical evidence suggests that the dorsal limbic division is (i) regulated preferentially by excitatory feedforward control, (ii) consolidated by REM sleep, and (iii) controlled in waking by phasic arousal through lemnothalamic projections from the pontine brainstem reticular activating system. The ventral limbic division and striatum, (i) organizes the inhibitory neurophysiology of NREM to (ii) consolidate explicit memory in sleep, (iii) operating in waking cognition under the same inhibitory feedback control supported by collothalamic tonic activation from the midbrain. We propose that (i) these dual (excitatory and inhibitory) systems alternate in the stages of sleep, and (ii) in waking they must be balanced—at criticality—to optimize the active inference that generates conscious experiences. Optimal Bayesian belief updating rests on balanced feedforward (excitatory predictive) and feedback (inhibitory corrective) control biases that play the role of prior and likelihood (i.e., sensory) precision. Because the excitatory (E) phasic arousal and inhibitory (I) tonic activation systems that regulate these dual limbic divisions have distinct affective properties, varying levels of elation for phasic arousal (E) and anxiety for tonic activation (I), the dual control systems regulate sleep and consciousness in ways that are adaptively balanced—around the entropic nadir of E–I criticality—for optimal self-regulation of consciousness and psychological health. Because they are emotive as well as motive control systems, these dual systems have unique qualities of feeling that may be registered as subjective experience.