Sensory Processing Across Conscious and Nonconscious Brain States: From Single Neurons to Distributed Networks for Inferential Representation

Neuronal activity is markedly different across brain states: it varies from desynchronized activity during wakefulness to the synchronous alternation between active and silent states characteristic of deep sleep. Surprisingly, limited attention has been paid to investigating how brain states affect sensory processing. While it was long assumed that the brain was mostly disconnected from external stimuli during sleep, an increasing number of studies indicates that sensory stimuli continue to be processed across all brain states—albeit differently. In this review article, we first discuss what constitutes a brain state. We argue that—next to global, behavioral states such as wakefulness and sleep—there is a concomitant need to distinguish bouts of oscillatory dynamics with specific global/local activity patterns and lasting for a few hundreds of milliseconds, as these can lead to the same sensory stimulus being either perceived or not. We define these short-lasting bouts as micro-states. We proceed to characterize how sensory-evoked neural responses vary between conscious and nonconscious states. We focus on two complementary aspects: neuronal ensembles and inter-areal communication. First, we review which features of ensemble activity are conducive to perception, and how these features vary across brain states. Properties such as heterogeneity, sparsity and synchronicity in neuronal ensembles will especially be considered as essential correlates of conscious processing. Second, we discuss how inter-areal communication varies across brain states and how this may affect brain operations and sensory processing. Finally, we discuss predictive coding (PC) and the concept of multi-level representations as a key framework for understanding conscious sensory processing. In this framework the brain implements conscious representations as inferences about world states across multiple representational levels. In this representational hierarchy, low-level inference may be carried out nonconsciously, whereas high levels integrate across different sensory modalities and larger spatial scales, correlating with conscious processing. This inferential framework is used to interpret several cellular and population-level findings in the context of brain states, and we briefly compare its implications to two other theories of consciousness. In conclusion, this review article, provides foundations to guide future studies aiming to uncover the mechanisms of sensory processing and perception across brain states.