Decreasing alertness modulates perceptual decision-making

ABSTRACT The ability to make decisions based on external information, prior knowledge and evidence, is a crucial aspect of cognition and may determine the success and survival of an organism. Despite extensive work on decision-making mechanisms/models, understanding the effects of alertness on neural and cognitive processes remain limited. Here we use electroencephalography and behavioural modelling to characterise cognitive and neural dynamics of perceptual decision-making in awake/low alertness periods in humans (14 male, 18 female) and characterise the compensatory mechanisms as alertness decreases. Well-rested human participants, changing between full-wakefulness and low alertness, performed an auditory tone-localisation task and its behavioural dynamics was quantified with psychophysics, signal detection theory and drift-diffusion modelling, revealing slower reaction times, inattention to the left side of space, and a lower rate of evidence accumulation in periods of low alertness. Unconstrained multivariate pattern analysis (decoding) showed a ~280ms delayed onset driven by low alertness of the neural signatures differentiating between left and right decision, with a spatial reconfiguration from centro-parietal to lateral frontal regions 150-360ms. To understand the neural compensatory mechanisms with decreasing alertness, we connected the evidence-accumulation behavioural parameter to the neural activity, showing in the early periods (125-325ms) a shift in the associated patterns from right parietal regions in awake, to right fronto-parietal during low alertness. This change in the neurobehavioural dynamics for central accumulation related cognitive processes define a clear reconfiguration of the brain networks’ regions and dynamics needed for the implementation of decision-making, revealing mechanisms of resilience of cognition when challenged by decreased alertness. Significance statement Most living organisms make multiple daily decisions and these require a degree of evidence from both the environment and the internal milieu. Such decisions are usually studied under sequential sampling models and involve making a behavioural choice based on sensory encoding, central accumulation, and motor implementation processes. Since there is little research on how decreasing alertness affects such cognitive processes, this study has looked at the cognitive and neural dynamics of perceptual decision-making in people while fully awake and in drowsy periods. Using computational modelling of behaviour and neural dynamics on human participants performing an auditory tone-localisation task, we reveal how low alertness modulates evidence accumulation related processes and its corresponding compensatory neural signatures.