The Yin and Yang of Sleep and Attention

Abstract

Sleep is not a single state, but a complex set of brain processes that supports several physiological needs. Sleep deprivation is known to affect attention in many animals, suggesting that a key function of sleep is to regulate attention. Conversely, tasks that require more attention drive sleep need and sleep intensity. Attention involves the ability to filter incoming stimuli based on their relative salience, and this is likely to require coordinated synaptic activity across the brain. This capacity may have only become possible with the evolution of related neural mechanisms that support two key sleep functions: stimulus suppression and synaptic plasticity. We argue here that sleep and attention may have coevolved as brain states that regulate each other.

Keywords: attention; brain; evolution; sleep.

Figure 1. Evolution of sleep and cognitive processes

As brains became more complex during evolution, animals gained the capacity for more sophisticated forms of cognition such as operant learning and selective attention (bottom yellow panel). At the same time, sleep evolved as a behavioural state that supported not only primitive functions such as stress and development, but also the plasticity needed for learning and attention (top yellow panel). Slow-wave sleep may be one mechanism to achieve synaptic plasticity and support cognition in mammals and birds, whereas this may be achieved in other animals by prolonged down-states in neural activity that occur during sleep. Importantly, sleep can be divided into two types: a primitive sleep-like state for stress responses and key developmental pathways which originated in animals with simpler nervous systems (e.g., certain nematodes, blue arrow) and a sleep state needed for the daily plasticity demands of cognition in animals with brains (e.g., from flies and molluscs to vertebrates, red arrow at the top of figure).

Figure 2. Sleep and attention are suppression states

A) In the nematode, C. elegans, sensory neurons display less spontaneous activity and reduced responses to external stimuli during sleep-like states, and B) the timing of neural responses within a circuit becomes less coordinated [26, 28]; during wake, stimulation of a sensory neuron (black circle) leads to synchronous firing of two different interneurons (grey circles), resulting in a motor response, whereas the output is suppressed during sleep-like behaviour due to a time-lag in one of the interneurons [26]. C) Sleep in the fruit fly Drosophila melanogaster is characterized by an overall suppression of neural activity recorded in the local field potential oscillations in the brain [56, 57]. D) In Drosophila, attention towards a visual stimulus coincides with an increase in 20-50 Hz oscillations in the brain, whereas the same oscillations are suppressed when the stimulus is ignored [36, 37]. E) In humans, wake is characterized by high frequency activity, whereas during slow-wave sleep, large amplitude slow-wave oscillations indicate prolonged up-states (neural activity) and down-states (suppression of neural activity). F) Alpha oscillations (8-13) Hz are thought to provide a gating mechanism for visual attention in humans; brain regions with low amplitude alpha oscillations correspond with attention to a stimulus, whereas high amplitude or phase shifted alpha oscillations suppress the processing of unattended stimuli [40, 42-45].