Aging Effect on Visuomotor Adaptation: Mediated by Cognitive Decline

The question of whether and how aging affects humans’ visuomotor adaptation remains controversial. This study investigates how the effect of aging on visuomotor adaptation is related to age-related cognitive declines. We compared the performance of 100 older people (age: 55–82 years) and 20 young adults (age: 18–27 years) on a visuomotor adaptation task and three cognition tasks. A decline in visuomotor adaptation of older people was well observed. However, this decline was not strongly correlated with chronological age increase but was associated to the age-related declines of cognitive functions and speed of motor planning. We then constructed a structural mediation model in which the declined cognitive resources mediated the effect of age increase on the decline in visuomotor adaptation. The data from the present study was well-explained by the mediation model. These findings indicate that the aging effect on visuomotor adaptation mainly reflects the age-related decline of cognitive functions, which results in insufficient explicit processing on visual perturbation during visuomotor control.

Visual perturbation of balance suggests impaired motor control but intact visuo-motor processing in Parkinson's disease

Postural instability marks one of the most disabling features of Parkinson's disease (PD), but only reveals itself after affected brain areas have already been significantly damaged. Thus, there is a need to detect deviations in balance and postural control before visible symptoms occur. In this study, we visually perturbed balance in the anterior-posterior direction using sinusoidal oscillations of a moving room in virtual reality at different frequencies. We tested three groups: individuals with PD under dopaminergic medication, an age-matched control group, and a group of young healthy adults. We tracked their centre of pressure and their full-body motion, from which we also extracted the centre of mass. We investigated sway amplitudes and applied newly introduced phase-locking analyses to investigate responses across participants' bodies. Patients exhibited significantly higher sway amplitudes as compared to the control subjects. However, their sway was phase-locked to the visual motion like that of age-matched and young healthy adults. Furthermore, all groups successfully compensated for the visual perturbation by phase-locking their sway to the stimulus. As frequency of the perturbation increased, distribution of phase-locking (PL) across the body revealed a shift of the highest PL-values from the upper body towards the hip-region for young healthy adults, which could not be observed in patients and elderly healthy adults. Our findings suggest an impaired motor control, but intact visuo-motor processing in early stages of PD, while less flexibility to adapt postural strategy to different perturbations revealed to be an effect of age rather than disease.

Visual perturbation of balance suggests impaired neuromuscular stability but intact visuo-motor control in Parkinson's disease

Postural instability marks one of the most disabling features of Parkinson's disease (PD), but only reveals itself after affected brain areas have already been significantly damaged. Thus, there is a need to detect deviations in balance and postural control before visible symptoms occur. In this study, we visually perturbed balance in the anterior-posterior direction using sinusoidal oscillations of a moving room in virtual reality at different frequencies. We tested three groups: individuals with PD under dopaminergic medication, an age-matched control group, and a group of young healthy adults. We tracked their centre of pressure and their full-body motion. We investigated sway amplitudes and applied newly introduced phase-locking analyses to investigate responses across participants' bodies. Patients exhibited significantly higher sway amplitudes as compared to the control subjects. However, their sway was phase-locked to the visual motion like that of age-matched and young healthy adults. Furthermore, all groups successfully compensated for the visual perturbation by - most likely reflexively - phase-locking their sway to the stimulus. As frequency of the perturbation increased, distribution of phase-locking (PL) across the body revealed a shift of the highest PL-values from the upper body towards the hip-region for young healthy adults, which could not be observed in patients and elderly healthy adults. Our findings suggest an impaired neuromuscular stability, but intact visuomotor processing in early stages of PD, while less flexibility to adapt postural strategy to different perturbations revealed to be an effect of age rather than disease.

Individual differences in proprioception predict the extent of implicit sensorimotor adaptation

Recent studies have revealed an upper bound in motor adaptation, beyond which other learning systems may be recruited. The factors determining this upper bound are poorly understood. The multisensory integration hypothesis states that this limit arises from opposing responses to visual and proprioceptive feedback. As individuals adapt to a visual perturbation, they experience an increasing proprioceptive error in the opposite direction, and the upper bound is the point where these two error signals reach an equilibrium. Assuming that visual and proprioceptive feedback are weighted according to their variability, there should be a correlation between proprioceptive variability and the limits of adaptation. Alternatively, the proprioceptive realignment hypothesis states that the upper bound arises when the (visually biased) sensed hand position realigns with the expected sensed position (target). When a visuo-proprioceptive discrepancy is introduced, the sensed hand position is biased towards the visual cursor, and the adaptive system counteracts this discrepancy by driving the hand away from the target. This hypothesis predicts a correlation between the size of the proprioceptive shift and the upper bound of adaptation. We tested these two hypotheses by considering natural variation in proprioception and motor adaptation across individuals. We observed a modest, yet reliable correlation between the upper bound of adaptation with both proprioceptive measures (variability and shift). While these results do not favor one hypothesis over the other, they underscore the critical role of proprioception in sensorimotor adaptation, and moreover, motivate a novel perspective on how these proprioceptive constraints drive implicit changes in motor behavior.

Eye-head coordination and dynamic visual scanning as indicators of visuo-cognitive demands in driving simulator

Driving is an everyday task involving a complex interaction between visual and cognitive processes. As such, an increase in the cognitive and/or visual demands can lead to a mental overload which can be detrimental for driving safety. Compiling evidence suggest that eye and head movements are relevant indicators of visuo-cognitive demands and attention allocation. This study aims to investigate the effects of visual degradation on eye-head coordination as well as visual scanning behavior during a highly demanding task in a driving simulator. A total of 21 emmetropic participants (21 to 34 years old) performed dual-task driving in which they were asked to maintain a constant speed on a highway while completing a visual search and detection task on a navigation device. Participants did the experiment with optimal vision and with contact lenses that introduced a visual perturbation (myopic defocus). The results indicate modifications of eye-head coordination and the dynamics of visual scanning in response to the visual perturbation induced. More specifically, the head was more involved in horizontal gaze shifts when the visual needs were not met. Furthermore, the evaluation of visual scanning dynamics, based on time-based entropy which measures the complexity and randomness of scanpaths, revealed that eye and gaze movements became less explorative and more stereotyped when vision was not optimal. These results provide evidence for a reorganization of both eye and head movements in response to increasing visual-cognitive demands during a driving task. Altogether, these findings suggest that eye and head movements can provide relevant information about visuo-cognitive demands associated with complex tasks. Ultimately, eye-head coordination and visual scanning dynamics may be good candidates to estimate drivers’ workload and better characterize risky driving behavior.

Individual differences in proprioception predict the extent of implicit sensorimotor adaptation

ABSTRACTRecent studies have revealed an upper bound in motor adaptation, beyond which other learning systems may be recruited. The factors determining this upper bound are poorly understood. The multisensory integration hypothesis states that this limit arises from opposing responses to visual and proprioceptive feedback. As individuals adapt to a visual perturbation, they experience an increasing proprioceptive error in the opposite direction, and the upper bound is the point where these two error signals reach an equilibrium. Assuming that visual and proprioceptive feedback are weighted according to their variability, there should be a correlation between proprioceptive variability and the limits of adaptation. Alternatively, the proprioceptive realignment hypothesis states that the upper bound arises when the (biased) sensed hand position realigns with the target. When a visuo-proprioceptive discrepancy is introduced, the sensed hand position is biased towards the visual cursor and the adaptive system nullifies this discrepancy by driving the hand away from the target. This hypothesis predicts a correlation between the size of the proprioceptive shift and the upper bound of adaptation. We tested these two hypotheses by considering natural variation in proprioception and motor adaptation across individuals. We observed a modest, yet reliable correlation between the upper bound of adaptation with both proprioceptive measures (variability and shift). While these results do not favor one hypothesis over the other, they underscore the critical role of proprioception in sensorimotor adaptation, and moreover, motivate a novel perspective on how these proprioceptive constraints drive implicit changes in motor behavior.SIGNIFICANCE STATEMENTWhile the sensorimotor system uses sensory feedback to remain properly calibrated, this learning process is constrained, limited in the maximum degree of plasticity. The factors determining this limit remain elusive. Guided by two hypotheses concerning how visual and proprioceptive information are integrated, we show that individual differences in the upper bound of adaptation in response to a visual perturbation can be predicted by the bias and variability in proprioception. These results underscore the critical, but often neglected role of proprioception in human motor learning.

Eye-head coordination and dynamic visual scanning as indicators of visuo-cognitive demands in driving simulator

Driving is an everyday task involving a complex interaction between visual and cognitive processes. As such, an increase in the cognitive and/or visual demands can lead to a mental overload which can be detrimental for driving safety. Compiling evidence suggest that eye and head movements are relevant indicators of visuo-cognitive demands and attention allocation. This study aims to investigate the effects of visual degradation on eye-head coordination as well as visual scanning behavior during a highly demanding task in a driving simulator. A total of 21 emmetropic participants (21 to 34 years old) performed dual-task driving in which they were asked to maintain a constant speed on a highway while completing a visual search and detection task on a navigation device. Participants did the experiment with optimal vision and with contact lenses that introduced a visual perturbation (myopic defocus). The results indicate modifications of eye-head coordination and the dynamics of visual scanning in response to the visual perturbation induced. More specifically, the head was more involved in horizontal gaze shifts when the visual needs were not met. Furthermore, the evaluation of visual scanning dynamics, based on time-based entropy which measures the complexity and randomness of scanpaths, revealed that eye and gaze movements became less explorative and more stereotyped when vision was not optimal. These results provide evidence for a reorganization of both eye and head movements in response to increasing visual-cognitive demands during a driving task. Altogether, these findings suggest that eye and head movements can provide relevant information about visuo-cognitive demands associated with complex tasks. Ultimately, eye-head coordination and visual scanning dynamics may be good candidates to estimate drivers’ workload and better characterize risky driving behavior.

Continuous Reports of Sensed Hand Position During Sensorimotor Adaptation

ABSTRACTSensorimotor learning entails multiple learning processes, some volitional and explicit, and others automatic and implicit. A new method to isolate implicit adaptation involves the use of a “clamped” visual perturbation in which, during a reaching movement, visual feedback is limited to a cursor that follows an invariant trajectory, offset from the target by a fixed angle. Despite full awareness that the cursor movement is not contingent on their behavior, as well as explicit instructions to ignore the cursor, systematic changes in motor behavior are observed, and these changes have the signatures of implicit adaptation observed in studies using classic visuomotor perturbations. While it is clear that the response to clamped feedback occurs automatically, it remains unknown if the adjustments in behavior remain outside the participant’s awareness. To address this question, we used the clamp method and directly probed awareness by asking participants to report their hand position after each reach. As expected, we observed robust deviations in hand angle away from the target (average of ∼18°). The hand reports also showed systematic deviations over the course of adaptation, initially attracted towards the visual feedback and then in the opposite direction, paralleling the shift in hand position. However, these effects were subtle (∼2° at asymptote), with the hand reports dominated by a feedforward signal associated with the motor intent yet modulated in a limited way by feedback sources. These results confirm that adaptation in response to a visual perturbation is not only automatic, but also largely implicit.NEWS AND NOTEWORTHYSensorimotor adaptation operates in an obligatory manner. Qualitatively, subjective reports obtained after adaptation demonstrate that, in many conditions, participants are unaware of significant changes in behavior. In the present study, we quantified participants’ awareness of adaptation by obtaining reports of hand position on a trial-by-trial basis. The results confirm that participants are largely unaware of adaptation, but also reveal the subtle influence of feedback on their subjective experience.