SummaryFrom the act of exploring an environment to that of grasping a cup of tea, animals must put in register their motor acts with their surrounding space. In the motor domain, this is likely to be defined by a register of three-dimensional (3D) displacement vectors, whose recruitment allows motion in the direction of a target. One such spatially targeted action is seen in the head reorientation behavior of mice, yet the neural mechanisms underlying these 3D behaviors remain unknown. Here, by developing a head-mounted inertial sensor for studying 3D head rotations and combining it with electrophysiological recordings, we show that neurons in the mouse superior colliculus are either individually or conjunctively tuned to the three Eulerian components of head rotation. The average displacement vectors associated with motor-tuned colliculus neurons remain stable over time and are unaffected by changes in firing rate or the duration of spike trains. Finally, we show that the motor tuning of collicular neurons is largely independent from visual or landmark cues. By describing the 3D nature of motor tuning in the superior colliculus, we contribute to long-standing debate on the dimensionality of collicular motor decoding; furthermore, by providing an experimental paradigm for the study of the metric of motor tuning in mice, this study also paves the way to the genetic dissection of the circuits underlying spatially targeted motion.

The level of alertness fluctuates throughout the day, exerting modulatory effects on human cognitive processes at any moment. However, our knowledge of how alertness level interacts with specific cognitive demands and perceptual rules of the task is still limited. Here we use perceptual decision-making paradigms to understand how alertness modulates the detection of a stimulus and the capacity to discriminate one stimulus from another. We analyzed data from four different experiments (113 participants in total): 1 - auditory masking detection; 2 - sensorimotor detection; 3 - auditory spatial discrimination; and 4 - auditory phoneme discrimination, and examined the performance of participants during the natural transition from awake (high alertness) to drowsy (low alertness). First, we fitted psychometric functions to the hit rates across different conditions of difficulty for EEG-defined high and low alertness metastable states, respectively. Second, we performed modelling of slope and threshold for the fitted curves as well as signal detection theory measures of perceptual sensitivity (d') and response bias (criterion). We found lower detection and discrimination sensitivity to stimuli as alertness level decreases, signalled by a shallower slope of the sigmoidal curve and a lower d', while the threshold increases slightly and equivalently across experiments during lower alertness. There was no change in the criterion to make the decision during the transition. These results suggest that reduced alertness generally decreases the quality of perceptual decision-making. Zooming in, we observed that the decrease in sensitivity measured by slope was stronger for discrimination than for detection decisions, indicating that lower alertness impairs the precision of decisions in discriminating alternatives more than identifying the presence of a stimulus around the threshold. Taken together, these results suggest that alertness has a common effect on perceptual decision-making and differentially modulates detection and discrimination decisions.

In a single day we transition from vigilant wakefulness to unconscious sleep and dreaming, undergoing diverse behavioural, physiological and neural changes. While during the awake state, exogenous stimuli and endogenous changes lead to sensory reorganisation, this remapping has not been charted throughout the sleep-wake cycle. We recorded neural activity in response to a range of tones using electroencephalography during a full-night sleep, and examined whether auditory responses become more similar, dissimilar or remain unchanged between wakefulness, non-rapid (NREM) and rapid eye movement (REM) sleep. We found that neural similarities between pairs of auditory evoked potentials differed by conscious state in both early and late auditory processing stages. Furthermore, tone-pairs neural similarities were modulated by conscious state as a function of tone frequency, where some tone-pairs changed similarity between states and others continued unaffected. These findings demonstrate a state-, stimulus- and time-dependent functional reorganization of auditory processing across the sleep-wake cycle.