Sleepwalkers’ complex nocturnal behaviors have inspired fictional characters from Shakespeare’s Lady Macbeth to Polidori’s Vampyre to Cesare, the homicidal somnambulist in The Cabinet of Dr Caligari. Yet although the underlying pathophysiology of sleepwalking, i.e. the partial arousal from slow-wave sleep, is today well-documented, the detailed sensorimotor mechanisms permitting locomotion and further complex behaviors to occur outside of conscious control remain poorly understood []. Further, the paroxysmal character, nocturnal pattern, and spontaneous onset have made it nigh on impossible to study somnambulism behaviorally during wakefulness. The goal-directed walking paradigm reported here, based on full-body motion capture and virtual reality feedback, directly addresses this issue and provides unique insights into the functional mechanisms of this common parasomnia: sleepwalkers exhibited improved movement automation and a stronger dissociation between locomotor control and awareness than matched controls when challenged with a cognitive load. Our data therefore suggest that behavioral markers exist in awake sleepwalkers, characterized by their ability to perform complex locomotor actions in the absence of full consciousness. Our findings are important as they firmly link sleepwalking to the neuroscience of motor control and motor awareness and may complement formal diagnosis procedures (normally requiring time, cost-intensive sleep studies and polysomnographic recordings).

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2 Wegner D.M. The Illusion of Conscious Will. 3 Blakemore S.J.

Wolpert D.M.

Frith C.D. Abnormalities in the awareness of action. 4 Fourneret P.

Jeannerod M. Limited conscious monitoring of motor performance in normal subjects. 5 Repp B.H.

Knoblich G. Toward a psychophysics of agency: detecting gain and loss of control over auditory action effects. 6 Yogev-Seligmann G.

Hausdorff J.M.

Giladi N. The role of executive function and attention in gait. 7 Kannape O.A.

Blanke O. Self in motion: sensorimotor and cognitive mechanisms in gait agency. 8 Kannape O.A.

Barré A.

Aminian K.

Blanke O. Cognitive loading affects motor awareness and movement kinematics but not locomotor trajectories during goal-directed walking in a virtual reality environment. Dissociations between automated motor control and awareness, so striking in each sleepwalking episode, have been extensively studied in healthy populations, albeit at much weaker dissociation levels []. Generally inspired by the comparator framework [], such paradigms quantify participants’ motor awareness and performance when exposed to different spatiotemporal mismatches concerning auditory or visual feedback about on-going movements []. Such paradigms have recently been adapted to locomotion, and in combination with dual tasking [] have illustrated an increased dissociation between locomotor control and awareness under cognitive load [].

8 Kannape O.A.

Barré A.

Aminian K.

Blanke O. Cognitive loading affects motor awareness and movement kinematics but not locomotor trajectories during goal-directed walking in a virtual reality environment. 6 Yogev-Seligmann G.

Hausdorff J.M.

Giladi N. The role of executive function and attention in gait. Figure 1 Effects of cognitive loading in sleepwalkers and control participants. Show full caption (A) Participants performed a goal-directed walking task in a virtual reality environment. Feedback could be veridical or deviated to the left or right by 5° to 30° (solid red line). (B) All participants correctly compensated for the introduced angular deviations to reach the virtual target location (left/right collapsed). Motor compensation did not differ between sleepwalkers (SW) and control participants. (C) Walking velocities were calculated for the initial step (0–30 cm), the main trajectory (30–150 cm), and the final step (150–180 cm) to remove initial freezing or hesitation at the end of the trial. Control participants significantly slowed down under cognitive loading, whereas sleepwalkers maintained their walking velocity. (D) At the end of each trial participants judged whether or not the movement shown on the screen corresponded to the movement they had just performed. These ratings were used to generate 50% motor awareness thresholds. Sleepwalkers’ and control participants’ awareness thresholds largely overlapped in the single task (ST) condition but were differently affected by cognitive loading (dual task, DT). While control participants over-attributed more deviated feedback trials in the dual task condition (solid red line), sleepwalkers correctly rejected more of these trials under cognitive load (dotted blue line, error bars μ ± SEM). To investigate both locomotor control and awareness in sleepwalkers, we asked a group of clinically diagnosed sleepwalkers and a group of age- and gender-matched control participants to move their tracked, virtual body into a virtual target cylinder by performing the corresponding goal-directed movement in the tracking arena ( Figure 1 A, see Experimental Procedures in Supplemental Information , published with this article online). Feedback of walking trajectories could be veridical or randomly deviated to the left/right by 5°–30° such that participants had to compensate for the deviation in order to reach the target []. Participants rated the veracity of the received feedback after each trial (yes/no). The secondary task was articulated backwards counting (steps of 7), a task reliably shown to interfere with locomotor control (independent of errors in arithmetic) [].

7 Kannape O.A.

Blanke O. Self in motion: sensorimotor and cognitive mechanisms in gait agency. 8 Kannape O.A.

Barré A.

Aminian K.

Blanke O. Cognitive loading affects motor awareness and movement kinematics but not locomotor trajectories during goal-directed walking in a virtual reality environment. 8 Kannape O.A.

Barré A.

Aminian K.

Blanke O. Cognitive loading affects motor awareness and movement kinematics but not locomotor trajectories during goal-directed walking in a virtual reality environment. All participants correctly performed the task and accurately identified that the virtual body reflected their own movements in control trials (93 ± 2% μ ± SEM self-attribution, cf. Table S1 ) and correctly rejected strongly deviated trials (4 ± 2% self-attribution for 30° mismatch, main effect of Deviation: P < 0.001), closely replicating previous results [] (Bayes factor analysis BF = 4.58, half-normal prior derived from []). As illustrated in Figure 1 D, there were no overt differences in locomotor awareness thresholds (controls: 13.4° ± 1.5, sleepwalkers: 13.2° ± 1.7) or walking performance (accuracy, velocity) between the groups in the single task condition.

However, under cognitive load, our study reveals two key findings that link sleepwalking to motor control and motor awareness in wakefulness. The first important finding is the sleepwalker’s ability to maintain the sequential locomotor pattern under cognitive load. Whereas walking velocity was significantly affected by cognitive loading overall (0.70 ± 0.15 m/s to 0.65 ± 0.14 m/s, P = 0.010), there was an interaction between factors Group and Task (P = 0.014). In line with clinical locomotion data, control participants significantly slowed down when performing the secondary task (0.68 ± 0.20 m/s to 0.59 ± 0.18 m/s, P < 0.001) whereas sleepwalkers maintained similar walking velocities across conditions (0.73 ± 0.22 m/s to 0.72 ± 0.21 m/s, P = 0.59, Figure 1 C). This suggests that the degree of walking automaticity in the present sleepwalkers differs from controls, as hypothesized (cf. Supplemental Experimental Procedures ).

7 Kannape O.A.

Blanke O. Self in motion: sensorimotor and cognitive mechanisms in gait agency. 8 Kannape O.A.

Barré A.

Aminian K.

Blanke O. Cognitive loading affects motor awareness and movement kinematics but not locomotor trajectories during goal-directed walking in a virtual reality environment. 8 Kannape O.A.

Barré A.

Aminian K.

Blanke O. Cognitive loading affects motor awareness and movement kinematics but not locomotor trajectories during goal-directed walking in a virtual reality environment. 9 Haggard P.

Martin F.

Taylor-Clarke M.

Jeannerod M.

Franck N. Awareness of action in schizophrenia. The second key finding is that sleepwalkers correctly rejected significantly more deviated trials under cognitive load than control participants. This is reflected in the opposing effects dual tasking had on the two cohorts: 50% awareness thresholds decreased to 10.5° ± 1.0 for sleepwalkers whereas thresholds increased to 16.5° ± 2.3 in the control group, in line with previous results in healthy participants [] (significant interaction Group by Task: P = 0.016; interaction BF = 15.70 using normal prior based on control participant data). We note that this change in sleepwalker locomotor awareness thresholds is unlike previous control [] or patient groups (such as persons with schizophrenia or de-afferented neurological patients) who tend to overly rate action-feedback as self-generated, particularly in trials with high ambiguity or uncertainty. Such attribution errors have been described as arising from sensory noise or, in the case of participants diagnosed with schizophrenia, impairments in the underlying comparator mechanism []. However, sleepwalkers showed the opposite response pattern and correctly rejected deviated feedback trials under cognitive load. These differences are also not explained by a difference in motor compensation (see Figure 1 B for example paths), as walking accuracy, measured at the trajectory endpoint, did not statistically differ significantly across the single and dual task conditions (P > 0.20). There was further no significant correlation between the walking velocity and the awareness thresholds (neither in the single-, dual-task condition, nor the aggregate, all P > 0.07), indicating that the locomotor awareness differences observed in the dual task condition are due to our experimental manipulation and not a change in walking characteristics.