Visuokinesthetic Realignment in a Video-Controlled Reaching Task

The authors investigated the accuracy of horizontal pointing movements toward a visual target viewed on a vertical video monitor; the view included a directional distortion between perceptual and action spaces. Although accurate coding of the movement vector in a relative (visual) system of coordinates has been found to occur when there is a prismatic perturbation, provided that the hand and the target are continuously visible, such accurate performance has never been reported for video-controlled situations with larger deviations. To evaluate whether visual relative coding is task specific or depends on the magnitude of the induced misalignment, the authors manipulated the intensity of directional perturbation (10° or 40°) in a video-controlled task. Whatever the directional bias, participants (N = 40) were initially inaccurate but adapted quickly within a few trial rehearsals, with a concomitant recalibration of segmental proprioception. In contrast with prism studies, relative coding of the hand-to-target vector seemed not to be operative in video-controlled situations, suggesting that target location is specified in an egocentric system of reference that includes hand-related proprioceptive signals, despite the presence of a (consciously) detected misalignment between visual and kinesthetic systems.     

An examination of the relationship between visual capture and prism adaptation

The phenomena of prismatically induced “visual capture” and adaptation of the hand were compared. In Experiment 1, it was demonstrated that when the subject’s hand was transported for him by the experimenter (passive movement) immediately preceding the measure of visual capture, the magnitude of the immediate shift in felt limb position (visual capture) was enhanced relative to when the subject moved the hand himself (active movement). In Experiment 2, where the dependent measure was adaptation of the prism-exposed hand, the opposite effect was produced by the active/passive manipulation. It appears, then, that different processes operate to produce visual capture and adaptation. It was speculated that visual capture represents an immediate weighting of visual over proprioceptive input as a result of the greater precision of vision and/or the subject’s tendency to direct his attention more heavily to this modality. In contrast, prism adaptation is probably a recalibration of felt limb position in the direction of vision, induced by the presence of a registered discordance between visual and proprioceptive inputs.     

Adaptation to visual and proprioceptive rearrangement: Origin of the differential effectiveness of active and passive movements

In Experiment 1, subjects exposed to a discordance between the visual and ”proprioceptive” locations of external targets were found to exhibit aftereffects when later pointing without sight of their hands at visual targets. Aftereffects occur both when the discordance is introduced in the traditional fashion by displacing the visual locations of targets and when the proprioceptive locations of targets are displaced. These observations indicate that there is nothing unique about the visual rearrangement paradigm—the crucial factor determining whether adaptation will be elicited is the presence of a discordance in the positional information being conveyed over two different sensory modalities. In a second experiment, the effectiveness of active and passive movements in eliciting adaptation was studied using an experimental paradigm in which subjects were exposed to a systematic discordance between the visual and proprioceptive locations of external targets without ever being permitted sight of their hands; a superiority of active movements was observed, just as is usually found in visual rearrangement experiments in which sight of the hand is permitted. Evidence is presented that the failure of passive movements to elicit adaptation is related to a deterioration in accuracy of position sense information during passive limb movement.     

Visuokinesthetic realignment in a video-controlled reaching task

The authors investigated the accuracy of horizontal pointing movements toward a visual target viewed on a vertical video monitor; the view included a directional distortion between perceptual and action spaces. Although accurate coding of the movement vector in a relative (visual) system of coordinates has been found to occur when there is a prismatic perturbation, provided that the hand and the target are continuously visible, such accurate performance has never been reported for video-controlled situations with larger deviations. To evaluate whether visual relative coding is task specific or depends on the magnitude of the induced misalignment, the authors manipulated the intensity of directional perturbation (10 degrees or 40 degrees) in a video-controlled task. Whatever the directional bias, participants (N = 40) were initially inaccurate but adapted quickly within a few trial rehearsals, with a concomitant recalibration of segmental proprioception. In contrast with prism studies, relative coding of the hand-to-target vector seemed not to be operative in video-controlled situations, suggesting that target location is specified in an egocentric system of reference that includes hand-related proprioceptive signals, despite the presence of a (consciously) detected misalignment between visual and kinesthetic systems.     

Prism adaptation changes the subjective proprioceptive localization of the hands

Prism adaptation involves a proprioceptive, a visual and a motor component. As the existing paradigms are not able to distinguish between these three components, the contribution of the proprioceptive component remains unclear. In the current study, a proprioceptive judgement task, in the absence of motor responses, was used to investigate how prism adaptation would specifically influences the felt position of the hands in healthy participants. The task was administered before and after adaptation to left and right displacing prisms using either the left or the right hand during the adaptation procedure. The results appeared to suggest that the prisms induced a drift in the felt position of the hands, although the after‐effect depended on the combination of the pointing hand and the visual deviation induced by prisms. The results are interpreted as in line with the hypothesis of an asymmetrical neural architecture of somatosensory processing. Moreover, the passive proprioception of the hand position revealed different effects of proprioceptive re‐alignment compared to active pointing straight ahead: different mechanisms about how visuo‐proprioceptive discrepancy is resolved were hypothesized.     

Telling the right hand from the left hand: multisensory integration, not motor imagery, solves the problem

Judging the laterality of a hand seen at unanticipated orientations evokes a robust feeling of bodily movement, even though no movement is produced. In two experiments, we tested a novel hypothesis to explain this phenomenon: A hand's laterality is determined via a multisensory binding of the visual representation of the seen hand and a proprioceptive representation of the observer's felt hand, and the felt "movement" is an obligatory aftereffect of intersensory recalibration. Consistent with the predictions implied by such a cross-modal mechanism, our results in Experiment 1 showed that manipulating observers' selective attention can evoke illusory feelings of movement in the "wrong" hand (i.e., the hand whose laterality does not match that of the stimulus). In Experiment 2, these illusions were readily extinguished in conditions in which binding was predicted to fail, a result indicating that cross-modal binding was necessary to produce them. These results are not explained by imagery, a mechanism widely assumed to account for how hand laterality is identified.     

Central fatigue mechanisms are responsible for decreases in hand proprioceptive acuity following shoulder muscle fatigue

Muscle fatigue is a complex phenomenon, consisting of central and peripheral mechanisms which contribute to local and systemic changes in motor performance. In particular, it has been demonstrated that afferent processing in the fatigued muscle (e.g., shoulder), as well as in surrounding or distal muscles (e.g., hand) can be altered by fatigue. Currently, it is unclear how proximal muscle fatigue affects proprioceptive acuity of the distal limb. The purpose of the present study was to assess the effects of shoulder muscle fatigue on participants’ ability to judge the location of their hand using only proprioceptive cues. Participants’ (N = 16) limbs were moved outwards by a robot manipulandum and they were instructed to estimate the position of their hand relative to one of four visual reference targets (two near, two far). This estimation task was completed before and after a repetitive pointing task was performed to fatigue the shoulder muscles. To assess central versus peripheral effects of fatigue on the distal limb, the right shoulder was fatigued and proprioceptive acuity of the left and right hands were tested. Results showed that there was a significant decrease in the accuracy of proprioceptive estimates for both hands after the right shoulder was fatigued, with no change in the precision of proprioceptive estimates. A control experiment (N = 8), in which participants completed the proprioceptive estimation task before and after a period of quiet sitting, ruled out the possibility that the bilateral changes in proprioceptive accuracy were due to a practice effect. Together, these results indicate that shoulder muscle fatigue decreases proprioceptive acuity in both hands, suggesting that central fatigue mechanisms are primarily responsible for changes in afferent feedback processing of the distal upper limb.     

Visuomotor Adaptation and Proprioceptive Recalibration

ABSTRACT

Motor learning, in particular motor adaptation, is driven by information from multiple senses. For example, when arm control is faulty, vision, touch, and proprioception can all report on the arm's movements and help guide the adjustments necessary for correcting motor error. In recent years we have learned a lot about how the brain integrates information from multiple senses for the purpose of perception. However, less is known about how multisensory data guide motor learning. Most models of, and studies on, motor learning focus almost exclusively on the ensuing changes in motor performance without exploring the implications on sensory plasticity. Nor do they consider how discrepancies in sensory information (e.g., vision and proprioception) related to hand position may affect motor learning. Here, we discuss research from our lab and others that shows how motor learning paradigms affect proprioceptive estimates of hand position, and how even the mere discrepancy between visual and proprioceptive feedback can affect learning and plasticity. Our results suggest that sensorimotor learning mechanisms do not exclusively rely on motor plasticity and motor memory, and that sensory plasticity, in particular proprioceptive recalibration, plays a unique and important role in motor learning.     

Effects on prism adaptation of duration and timing of visual feedback during pointing

In two experiments, we investigated the effects of duration of visual feedback of the pointing limb and the time (early to late) in the movement when the limb first becomes visible (timing of visual feedback). Timing, rather than duration of visual feedback, proved to have the greater effect on the relative magnitude of visual and proprioceptive adaptation. Visual adaptation increased smoothly with feedback delay, but corresponding decreases in proprioceptive adaptation underwent an additional sharp change when feedback was delayed until about three-fourths of the way to the terminal limb position. These results are consistent with the idea that visual and proprioceptive adaptation are mediated by exclusive processes. Change in the limb position sense (i.e., proprioceptive adaptation) may be produced by visual guidance of the pointing limb, and view of the limb early in the pointing movement seems to be critical for such visual guidance. The limb may be ballistically released as it nears the terminal position, and, thereafter, any opportunity for visual guidance (i.e., view of the limb) is not effective. On the other hand, change in the eye position sense (i.e., visual adaptation) may be mediated by proprioceptive guidance of the eye; the eyes may track the imaged position of the nonvisible limb. Such proprioceptive guidance seems to be solely a function of the distance moved before the limb becomes visible.     

Effects on Prism Adaptation of Duration and Timing of Visual Feedback During Pointing

In two experiments, we investigated the effects of duration of visual feedback of the pointing limb and the time (early to late) in the movement when the limb first becomes visible (timing of visual feedback). Timing, rather than duration of visual feedback, proved to have the greater effect on the relative magnitude of visual and proprioceptive adaptation. Visual adaptation increased smoothly with feedback delay, but corresponding decreases in proprioceptive adaptation underwent an additional sharp change when feedback was delayed until about three-fourths of the way to the terminal limb position. These results are consistent with the idea that visual and proprioceptive adaptation are mediated by exclusive processes. Change in the limb position sense (i.e., proprioceptive adaptation) may be produced by visual guidance of the pointing limb, and view of the limb early in the pointing movement seems to be critical for such visual guidance. The limb may be ballistically “released“ as it nears the terminal position, and, thereafter, any opportunity for visual guidance (i.e., view of the limb) is not effective. On the other hand, change in the eye position sense (i.e., visual adaptation) may be mediated by proprioceptive guidance of the eye; the eyes may track the imaged position of the nonvisible limb. Such proprioceptive guidance seems to be solely a function of the distance moved before the limb becomes visible.     

The influence of embodiment on multisensory integration using the mirror box illusion

We examined the relationship between subcomponents of embodiment and multisensory integration using a mirror box illusion. The participants’ left hand was positioned against the mirror, while their right hidden hand was positioned 12″, 6″, or 0″ from the mirror – creating a conflict between visual and proprioceptive estimates of limb position in some conditions. After synchronous tapping, asynchronous tapping, or no movement of both hands, participants gave position estimates for the hidden limb and filled out a brief embodiment questionnaire. We found a relationship between different subcomponents of embodiment and illusory displacement towards the visual estimate. Illusory visual displacement was positively correlated with feelings of deafference in the asynchronous and no movement conditions, whereas it was positive correlated with ratings of visual capture and limb ownership in the synchronous and no movement conditions. These results provide evidence for dissociable contributions of different aspects of embodiment to multisensory integration.     

Visual and Proprioceptive Adaptation of Arm Position in a Virtual Environment

The authors examined the resolution of a discrepancy between visual and proprioceptive estimates of arm position in 10 participants. The participants fixed their right shoulder at 0°, 30°, or 60° of transverse adduction while they viewed a video on a head-mounted display that showed their right arm extended in front of the trunk for 30 min. The perceived arm position more closely approached the seen arm position on the display as the difference between the actual and visually displayed arm positions increased. In the extreme case of a 90° discrepancy, the seen arm position on the display was very gradually perceived as approaching the actual arm position. The magnitude of changes in sensory estimates was larger for proprioception (20%) than for vision (< 10%).     

Adaptation to prism-displaced vision: The importance of target-pointing

Two experiments investigated the hypothesis that the experience of manually pointing at visual targets enhances motoric adaptation to prism-displaced vision. Experiment 1 indicated that when adaptation was measured by means of redirected pointing behavior (negative aftereffect) it varied directly with the specificity of the target, the least adaptation occurring when no target was available. This relationship was not observed when adaptation was measured in terms of a shift in the felt position of the prism-exposed hand (proprioceptive shift). Experiment 2 demonstrated that after double the prism-exposure trials used in Experiment 1, target-pointing experience continued to enhance adaptation (as indexed by both types of adaptation measure). In both experiments negative aftereffect was significantly larger than proprioceptive shift for all experimental conditions and the two measures were not correlated. These latter two findings cast doubt on Harris’s notion that negative aftereffect is entirely the result of altered position sense.     

Development of forward models for hand localization and movement control in 6- to 10-year-old children

An active kinesthetic-to-visual matching task was performed by 15 children aged 5-10 years and five young adults. The task required the participants to locate the target visually while performing center-out drawing movements to the located visual targets in the absence of visual feedback of hand/pen motion. Movement time (MT), terminal end-point position error (EPE), and initial directional error (IDE) were measured. The general finding is that the end-point error variability, representing the joint localization probability distributions for proprioceptive localization of the hand and visual localization of the target, was largest for the youngest children, but did not differ from one another for the older age groups. The localization distributions, as characterized by principal component analysis, showed that both errors in extent and direction were significantly larger in the youngest children. These error distributions could not be accounted for by initial localization errors prior to movement onset in the children. It is likely that at least some portion of the increased movement variability seen during sensorimotor development in young children can be attributed not only to immature control mechanisms per se, but also to partial, not yet stable, forward representations for hand localization which are used for movement perception, planning, and control.     

Adaptive Mechanisms in Perceptual-Motor Coordination

Aftereffect measures of visual shift and proprioceptive shift were obtained for prism exposure conditions in which, at the end of a sagittal pointing movement, most of the arm was visible (concurrent exposure) or only the first finger joint was visible (terminal exposure). Intermediate exposure conditions permitted view of the hand or the first two finger joints. Under the concurrent exposure condition, proprioceptive shift was greater than visual shift but, as view of the pointing hand decreased, the relative magnitude of the two components gradually reversed so that, under the terminal exposure condition, visual shift was greater than proprioceptive shift. These results are discussed in terms of a model of perceptual-motor organization (Redding, Clark, & Wallace, 1985) in which the direction of coordinative linkage between eye-head and hand-head systems determines the locus of discordance and adaptive recalibration.     

Adaptive mechanisms in perceptual-motor coordination: components of prism adaptation

Aftereffect measures of visual shift and proprioceptive shift were obtained for prism exposure conditions in which, at the end of a sagittal pointing movement, most of the arm was visible (concurrent exposure) or only the first finger joint was visible (terminal exposure). Intermediate exposure conditions permitted view of the hand or the first two finger joints. Under the concurrent exposure condition, proprioceptive shift was greater than visual shift but, as view of the pointing hand decreased, the relative magnitude of the two components gradually reversed so that, under the terminal exposure condition, visual shift was greater than proprioceptive shift. These results are discussed in terms of a model of perceptual-motor organization (Redding, Clark, & Wallace, 1985) in which the direction of coordinative linkage between eye-head and hand-head systems determines the locus of discordance and adaptive recalibration.     

Control of Rapid Arm Movements When Target Position Is Altered During Saccadic Suppression

This experiment examined whether rapid arm movements can be corrected in response to a change in target position that occurs just prior to movement onset, during saccadic suppression of displacement. Because the threshold of retinal input reaches its highest magnitude at that time, displacement of the visual target of a saccade is not perceived. Subjects (N = 6) were instructed to perform very rapid arm movements toward visual targets located 16, 20, and 24 degrees from midline (on average, movement time was 208 ms). On some trials the 20 degrees target was displaced 4 degrees either to the right or to the left during saccadic suppression. For double-step trials, arm movements did not deviate from their original trajectory. Movement endpoints and movement structure (i.e., velocity-and acceleration-time profiles) were similar whether or not target displacements occurred, showing the failure of proprioceptive signals or internal feedback loops to correct the arm trajectory. Following this movement, terminal spatially oriented movements corrected the direction of the initial movement (as compared with the single-step control trials) when the target eccentricity decreased by 4 degrees. Subjects were unaware of these spatial corrections. Therefore, spatial corrections of hand position were driven by the goal level of the task, which was updated by oculomotor corrective responses when a target shift occurred.     

Effects of Pointing Rate and Availability of Visual Feedback on Visual and Proprioceptive Components of Prism Adaptation

While looking through laterally displacing prisms, subjects pointed 60 times straight ahead of their nose at a rate of one complete movement every 2 or 3 s, with visual feedback available early in the pointing movement or delayed until the end of the movement. Sagittal pointing was paced such that movement speed covaried with pointing rate. Aftereffect measures (obtained after every 10 pointing trials) showed that when the limb became visible early in a pointing movement, proprioceptive adaptation was greater than visual, but when visual feedback was delayed until the end of the movement, the reverse was true. This effect occurred only with the 3-s pointing rate, however. With the 2-s pointing rate, adaptation was predominately proprioceptive in nature, regardless of feedback availability. Independent of the availability of visual feedback, visual adaptation developed more quickly with 3-s pointing, whereas proprioceptive adaptation developed more rapidly with 2-s pointing. These results are discussed in terms of a model of perceptual-motor organization in which the direction of coordinative (guidance) linkage between eye-head (visual) and hand-head (proprioceptive) systems (and consequently the locus of discordance registration and adaptive recalibration) is determined jointly by pointing rate and feedback availability. An additional effect of pointing rate is to determine the rate of discordant inputs. Maximal adaptive recalibration occurs when the input (pointing) rate matches the time constant of the adaptive encoder in the guided system.     

Repetitive pointing to remembered proprioceptive targets improves 3D hand positioning accuracy

Repetitive pointing movements to remembered proprioceptive targets were investigated to determine whether dynamic proprioception could be used to modify the initial sensorimotor conditions associated with an active definition of the target position. Twelve blindfolded subjects used proprioception to reproduce a self-selected target position as accurately as possible. Ten repetitions for each limb were completed using overhead and scapular plane pointing tasks. A 3D optical tracking system determined hand trajectory start and endpoint positions for each repetition. These positions quantified three-dimensional pointing errors relative to the target position and the initial and preceding movement repetitions, as well as changes in movement direction and extent. Target position and cumulative start position errors were significantly greater than the corresponding preceding movement (inter-repetition) errors, and increased as the trial progressed. In contrast, hand trajectory start and endpoint inter-repetition errors decreased significantly with repeated task performance, as did movement extent, although it was consistently underestimated for each repetition. Pointing direction remained constant, except for the angle of elevation for scapular plane pointing, which consistently decreased throughout the trial. The results suggest that the initial conditions prescribed by actively defining a proprioceptive target were subsequently modified by dynamic proprioception, such that movement reproduction capability improved with repeated task performance.     

Concurrent Directional Adaptation of Reactive Saccades and Hand Movements to Target Displacements of Different Size

When eye and hand movements are concurrently aimed at double-step targets that call for equal and opposite changes of response direction (–10° for the eyes, +10° for the hand), adaptive recalibration of both motor systems is strongly attenuated; instead, hand but not eye movements are changed by corrective strategies (V. Grigorova et al., 2013a). The authors introduce a complementary paradigm, where double-step targets call for a –10° change of eye and a ?30° change for hand movements. If compared to control subjects adapting only the eyes or only the hand, adaptive improvements were comparable for the eyes but were twice as large for the hand; in contrast, eye and hand aftereffects were comparable to those in control subjects. The authors concluded that concurrent exposure of eyes and hand to steps of the same direction but different size facilitated hand strategies, but didn't affect recalibration. This finding together with previous one (V. Grigorova et al., 2013a), suggests that concurrent adaptation of eyes and hand reveals different mechanisms of recalibration for step sign and step size, which are shared by reactive saccades and hand movements. However, hand mostly benefits from strategies provoked by the difference in target step sign and size.