Proprioceptive Cues Research Articles

The kinaesthetic mirror illusion: How much does the mirror matter?

The reflection of a moving hand in a mirror positioned in the sagittal plane can create an illusion of symmetrical, bimanual movement. This illusion is implicitly presumed to be of visual origin. However, muscle proprioceptive afferents of the arm reflected in the mirror might also affect the perceived position and movement of the other arm. We characterized the relative contributions of visual and proprioceptive cues by performing two experiments. In Experiment 1, we sought to establish whether kinaesthetic illusions induced using the mirror paradigm would survive marked visual impoverishment (obtained by covering between 0 and 100% of the mirror in 16% steps). We found that the mirror illusion was only significantly influenced when the visual degradation was 84% or more. In Experiment 2, we masked the muscle proprioceptive afferents of the arm reflected in the mirror by co-vibrating antagonistic muscles. We found that masking the proprioceptive afferents reduced the velocity of the illusory displacement of the other arm. These results confirm that the mirror illusion is not a purely visual illusion but emerges from a combination of congruent signals from the two arms, i.e. visual afferents from the virtually moving arm and proprioceptive afferents from the contralateral, moving arm.

Motor Gains from Using Proprioceptive Cues in Treadmill Walking: Clinical Exercise Rehabilitation for Individuals with Parkinson’s Disease

Treadmill walking is the conventional rehabilitation strategy used to improve gait and stability in individuals with Parkinson’s disease. Current evidence suggests that coupling proprioceptive cues (such as vision and hearing) with treadmill walking can significantly improve measures of gait. Consistent with the model of the lifespan approach of motor development, these findings offer novel insight into rehabilitation strategies that have the potential to improve physical activity participation in individuals with Parkinson’s disease.

Increasing cutaneous afferent feedback improves proprioceptive accuracy at the knee in patients with sensory ataxia

Hereditary sensory and autonomic neuropathy type III (HSAN III) features disturbed proprioception and a marked ataxic gait. We recently showed that joint angle matching error at the knee is positively correlated with the degree of ataxia. Using intraneural microelectrodes, we also documented that these patients lack functional muscle spindle afferents but have preserved large-diameter cutaneous afferents, suggesting that patients with better proprioception may be relying more on proprioceptive cues provided by tactile afferents. We tested the hypothesis that enhancing cutaneous sensory feedback by stretching the skin at the knee joint using unidirectional elasticity tape could improve proprioceptive accuracy in patients with a congenital absence of functional muscle spindles. Passive joint angle matching at the knee was used to assess proprioceptive accuracy in 25 patients with HSAN III and 9 age-matched control subjects, with and without taping. Angles of the reference and indicator knees were recorded with digital inclinometers and the absolute error, gradient, and correlation coefficient between the two sides calculated. Patients with HSAN III performed poorly on the joint angle matching test [mean matching error 8.0 ± 0.8° (±SE); controls 3.0 ± 0.3°]. Following application of tape bilaterally to the knee in an X-shaped pattern, proprioceptive performance improved significantly in the patients (mean error 5.4 ± 0.7°) but not in the controls (3.0 ± 0.2°). Across patients, but not controls, significant increases in gradient and correlation coefficient were also apparent following taping. We conclude that taping improves proprioception at the knee in HSAN III, presumably via enhanced sensory feedback from the skin.

Roles of an Upper-Body Compression Garment on Athletic Performances

Compression garments (CGs) have been previously shown to enhance proprioception; however, this benefit has not been previously shown to transfer to improved performance in sports skills. The purpose of this study was to assess whether enhanced proprioception and comfort can be manifested in improved sports performance of high-level athletes. Eleven Division I collegiate pitchers (age: 21.0 ± 2.9 years; height: 181.0 ± 4.6 cm; weight: 89.0 ± 13.0 kg; body fat: 12.0 ± 4.1%) and 10 Division I collegiate golfers (age: 20.0 ± 1.3 years; height: 178.1 ± 3.9 cm; weight: 76.4 ± 8.3 kg; body fat: 11.8 ± 2.6%) participated in the study. A counterbalanced within-group design was used. Subjects performed the respective baseball or golf protocol wearing either typical noncompressive (NC) or the experimental CG. Golfers participated in an assessment of driving distance and accuracy, as well as approach shot, chipping, and putting accuracy. Pitchers were assessed for fastball accuracy and velocity. In pitchers, there was a significant (p ≤ 0.05) improvement in fastball accuracy (NC: 0.30 ± 0.04 vs. CG: 0.21 ± 0.07 cm). There were no differences in pitching velocity. In golfers, there were significant (p ≤ 0.05) improvements in driving accuracy (NC: 86.7 ± 30.6 vs. CG: 68.9 ± 18.5 feet), as well as approach shot accuracy (NC: 26.6 ± 11.9 vs. CG: 22.1 ± 8.2 feet) and chipping accuracy (NC: 2.9 ± 0.6 vs. CG: 2.3 ± 0.6 inch). There was also a significant (p ≤ 0.05) increase in comfort for the golfers (NC: 3.7 ± 0.8 vs. CG: 4.5 ± 1.0). These results demonstrate that comfort and performance can be improved with the use of CGs in high-level athletes being most likely mediated by improved proprioceptive cues during upper-body movements.

Combining visual and proprioceptive cues to improve the discrimination of object location

Combining visual and proprioceptive cues to improve the discrimination of object location

Mediterranean storm petrels rely on nest position for homing after migration: a test with artificial nestboxes

Petrels are highly philopatric and return from migratory journeys of thousands of kilometres to breed in the same burrow year after year. During the breeding season, some burrowing petrel species rely on their sense of smell to locate their nest at night, but the mechanisms involved in the homing behaviour after several months at sea are virtually unknown. To understand whether the sense of smell is involved in nest finding at the return from migration and to study the interplay with other positional cues, we explored the homing behaviour and nest choice by Mediterranean storm petrels, Hydrobates pelagicus melitensis. During two consecutive winters, we conducted our research in a colony with well-used artificial nestboxes that has been studied for the past two decades. We experimentally displaced previously occupied nestboxes in late winter and then checked for nest choice and occupancy by breeding individuals in the following breeding season. This experimental design allowed the manipulation of the location of the burrow, and the olfactory information contained within, without manipulating other positional cues. We observed that almost all individuals nested in the nestbox located at the same position as the year before, regardless of whether the nestbox was the one they had previously occupied or another one. During the breeding period, we also tested in a Y-maze the olfactory preference for the occupied nestbox with respect to another random one. Again, storm petrels did not show any olfactory preference for their nest. Our study implies that storm petrels breeding in a cave rely on other positional cues than olfactory ones to home and suggests a mechanism combining tactile and proprioceptive cues to find the nest in the dark.

The effect of hand movements on numerical bisection judgments in early blind and sighted individuals

Recent evidence suggests that in representing numbers blind individuals might be affected differently by proprioceptive cues (e.g., hand positions, head turns) than are sighted individuals. In this study, we asked a group of early blind and sighted individuals to perform a numerical bisection task while executing hand movements in left or right peripersonal space and with either hand. We found that in bisecting ascending numerical intervals, the hemi-space in which the hand was moved (but not the moved hand itself) influenced the bisection bias similarly in both early blind and sighted participants. However, when numerical intervals were presented in descending order, the moved hand (and not the hemi-space in which it was moved) affected the bisection bias in all participants. Overall, our data show that the operation to be performed on the mental number line affects the activated spatial reference frame, regardless of participants' previous visual experience. In particular, both sighted and early blind individuals' representation of numerical magnitude is mainly rooted in world-centered coordinates when numerical information is given in canonical orientation (i.e., from small to large), whereas hand-centered coordinates become more relevant when the scanning of the mental number line proceeds in non-canonical direction.

Updating and orientation in auditory space

For stable sound localization in space, a listener has to account for self-motion. This requires a head-to-world coordinate transformation by combining proprioceptive and vestibular inputs with the binaural cues for sound localization. Proprioceptive and vestibular information influence the evaluation of spatial auditory cues as indicated by the numerous proprioceptive and vestibular neural inputs into the auditory brainstem. First, we evaluate the relative influence of vestibular and proprioceptive cues on updating the world-centered position of auditory targets during active and passive head and/or body rotations in azimuth. Our results show that both vestibular and proprioceptive signals are used to update the spatial representations of auditory targets, but that vestibular inputs contribute more than proprioceptive inputs. Second, we explore the interplay of spatial audition and self-motion in subjects for which auditory space evaluation is of utmost importance, namely, for blind humans relying on ech...

Untangling visual and proprioceptive contributions to hand localisation over time.

Previous studies showed that self-localisation ability involves both vision and proprioception, integrated into a single percept, with the tendency to rely more heavily on visual than proprioceptive cues. Despite the increasing evidence for the importance of vision in localising the hands, the time course of the interaction between vision and proprioception during visual occlusion remains unclear. In particular, we investigated how the brain weighs visual and proprioceptive information in hand localisation over time when the visual cues do not reflect the real position of the hand. We tested three hypotheses: Self-localisations are less accurate when vision and proprioception are incongruent; under the same conditions of incongruence, people first rely on vision and gradually revert to proprioception; if vision is removed immediately prior to hand localisation, accuracy increases. Sixteen participants viewed a video of their hands, under three conditions each undertaken with eyes open or closed: Incongruent conditions (right hand movement seen: inward, right hand real movement: outward), Congruent conditions (movement seen congruent to real movement). The right hand was then hidden from view and participants performed a localisation task whereby a moving vertical arrow was stopped when aligned with the felt position of their middle finger. A second experiment used identical methodology, but with the direction of the arrow switched. Our data showed that, in the Incongruent conditions (both with eyes open and closed), participants perceived their right hand close to its last seen position. Over time, the perceived position of the hand shifted towards the physical position. Closing the eyes before the localisation task increased the accuracy in the Incongruent condition. Crucially, Experiment 2 confirmed the findings and showed that the direction of arrow movement had no effect on hand localisation. Our hypotheses were supported: When vision and proprioception were incongruent, participants were less accurate and initially relied on vision and then proprioception over time. When vision was removed, this shift occurred more quickly. Our findings are relevant in understanding the normal and pathological processes underpinning self-localisation.

Bogus Visual Feedback Alters Onset of Movement-Evoked Pain in People With Neck Pain

Pain is a protective perceptual response shaped by contextual, psychological, and sensory inputs that suggest danger to the body. Sensory cues suggesting that a body part is moving toward a painful position may credibly signal the threat and thereby modulate pain. In this experiment, we used virtual reality to investigate whether manipulating visual proprioceptive cues could alter movement-evoked pain in 24 people with neck pain. We hypothesized that pain would occur at a lesser degree of head rotation when visual feedback overstated true rotation and at a greater degree of rotation when visual feedback understated true rotation. Our hypothesis was clearly supported: When vision overstated the amount of rotation, pain occurred at 7% less rotation than under conditions of accurate visual feedback, and when vision understated rotation, pain occurred at 6% greater rotation than under conditions of accurate visual feedback. We concluded that visual-proprioceptive information modulated the threshold for movement-evoked pain, which suggests that stimuli that become associated with pain can themselves trigger pain.

Continuous Spontaneous Alternation and Turn Alternation in Artemia sp.

Free-running spontaneous alternation refers to the animal’s tendency to prefer the least recently visited locations in successive spatial choices, which is attributed to the animals’ choice between stimuli based on prior experience. Turn alternation, which is observed in directional choices preceded by a forced turn in one direction, also reflects the animals’ tendency to alternate between directional choices but this tendency has been assumed to rely on other cues (e.g., proprioceptive cues) derived from the prior responses (e.g., forced turn in one direction). Based on previous studies, the turn alternation appears to rely on more primitive (lower-form) information features and to be a more frequently observed empirical phenomenon than the spontaneous alternation. We investigated these two behavioral alternation tendencies in Artemia sp. Experiment 1 tested the continuous spontaneous alternation (cSAB) performance of Artemia sp. in two different mazes: t-maze (three options) and plus maze (four options). Experiment 2 tested the turn alternation performance of Artemia sp. counter-balancing the direction of initial forced-turn between subjects. Our results showed that Artemia sp. had nearly chance level spontaneous alternation performance in the t-maze and plus maze whereas a higher than chance level turn alternation performance. These results support the ubiquity of turn alternation tendency across species and point at the lack of spontaneous alternation in Artemia sp.

Self-motion facilitates echo-acoustic orientation in humans.

The ability of blind humans to navigate complex environments through echolocation has received rapidly increasing scientific interest. However, technical limitations have precluded a formal quantification of the interplay between echolocation and self-motion. Here, we use a novel virtual echo-acoustic space technique to formally quantify the influence of self-motion on echo-acoustic orientation. We show that both the vestibular and proprioceptive components of self-motion contribute significantly to successful echo-acoustic orientation in humans: specifically, our results show that vestibular input induced by whole-body self-motion resolves orientation-dependent biases in echo-acoustic cues. Fast head motions, relative to the body, provide additional proprioceptive cues which allow subjects to effectively assess echo-acoustic space referenced against the body orientation. These psychophysical findings clearly demonstrate that human echolocation is well suited to drive precise locomotor adjustments. Our data shed new light on the sensory–motor interactions, and on possible optimization strategies underlying echolocation in humans.

Full body action remapping of peripersonal space: The case of walking

The space immediately surrounding the body, i.e. peripersonal space (PPS), is represented by populations of multisensory neurons, from a network of premotor and parietal areas, which integrate tactile stimuli from the body’s surface with visual or auditory stimuli presented within a limited distance from the body. Here we show that PPS boundaries extend while walking. We used an audio–tactile interaction task to identify the location in space where looming sounds affect reaction time to tactile stimuli on the chest, taken as a proxy of the PPS boundary. The task was administered while participants either stood still or walked on a treadmill. In addition, in two separate experiments, subjects either received or not additional visual inputs, i.e. optic flow, implying a translation congruent with the direction of their walking. Results revealed that when participants were standing still, sounds boosted tactile processing when located within 65–100cm from the participants’ body, but not at farther distances. Instead, when participants were walking PPS expands as reflected in boosted tactile processing at ~1.66m. This was found despite the fact the spatial relationship between the participant’s body and the sound’s source did not vary between the Standing and the Walking condition. This expansion effect on PPS boundaries due to walking was the same with or without optic flow, suggesting that kinematics and proprioceptive cues, rather than visual cues, are critical in triggering the effect. These results are the first to demonstrate an adaptation of the chest’s PPS representation due to whole body motion and are compatible with the view that PPS constitutes a dynamic sensory–motor interface between the individual and the environment.

Sensory integration during reaching: the effects of manipulating visual target availability.

When using visual and proprioceptive information to plan a reach, it has been proposed that the brain combines these cues to estimate the object and/or limb's location. Specifically, according to the maximum-likelihood estimation (MLE) model, sensory inputs are combined such that more reliable inputs are assigned a greater weight (Ernst and Banks in Nature 415:429-433, 2002). In this paper, we examined if the brain is able to adjust which sensory cue it weights the most. Specifically, we asked if the brain changes how it weights sensory information when the availability of a visual cue is manipulated. Twelve healthy subjects reached to visual (V), proprioceptive (P), or visual + proprioceptive (VP) targets under different visual delay conditions (e.g., on V and VP trials, the visual target was available for the entire reach; it was removed with the go signal, or it was removed 1 s before the go signal). To establish which sensory cue subjects weighted the most, we compared endpoint positions achieved on V and P reaches to VP reaches. Results indicated that subjects combined visual and proprioceptive cues in accordance with the MLE model when reaching to VP targets. Moreover, subjects' reaching errors to visual targets increased with longer visual delays (particularly in the vertical direction). However, there was no change in reach variability with longer delays, and subjects did not reweight visual information as the availability of visual information was manipulated. Thus, a change in visual environment is not sufficient to cause the brain to reweight how it processes sensory information.

Behavioral correlates of complex spike synchrony in cerebellar microzones.

The olivo-cerebellar system is crucial for smooth and well timed execution of movements based on sensory and proprioceptive cues. The inferior olive (IO) plays a pivotal role in this process by synchronizing its activity across neurons internally through connexin36 gap junctions and providing a timing and/or learning signal to the cerebellum. Even though synchrony achieved through electrical coupling in IO cells is generally thought to be important in timing motor output, a direct relation between timing of movement and synchrony of olivary discharges has never been demonstrated within functional microcomplexes using transgenics. Here we combined in vivo, two-photon calcium imaging of complex spikes in microcomplexes of Purkinje cell (PC) dendrites with high-speed filming of tail, trunk, and limb movements in awake wild-type and connexin36-deficient mice. In wild types at rest, functional clusters of PCs were poorly defined with synchrony correlations that were relatively small and spatially limited to mediolateral distances of ∼50 μm, whereas during locomotion synchrony of the same PCs increased in strength and extended over distances spanning multiple microzones that could be correlated to specific components of sharp and well bounded movements. Instead, connexin36-deficient mice exhibited prolonged and desynchronized complex spike activity within PC microcomplexes both at rest and during behavior. Importantly, the mutants also showed concomitant abnormalities in the execution of spinocerebellar reflexes, which were significantly slower and more gradual than in wild-type littermates, particularly following sensory perturbations. Our results highlight the importance of modulation of synchronous activity within and between cerebellar microcomplexes in on-line temporal processing of motor output.

Contributions of visual and proprioceptive information to travelled distance estimation during changing sensory congruencies.

Recent research has provided evidence that visual and body-based cues (vestibular, proprioceptive and efference copy) are integrated using a weighted linear sum during walking and passive transport. However, little is known about the specific weighting of visual information when combined with proprioceptive inputs alone, in the absence of vestibular information about forward self-motion. Therefore, in this study, participants walked in place on a stationary treadmill while dynamic visual information was updated in real time via a head-mounted display. The task required participants to travel a predefined distance and subsequently match this distance by adjusting an egocentric, in-depth target using a game controller. Travelled distance information was provided either through visual cues alone, proprioceptive cues alone or both cues combined. In the combined cue condition, the relationship between the two cues was manipulated by either changing the visual gain across trials (0.7×, 1.0×, 1.4×; Exp. 1) or the proprioceptive gain across trials (0.7×, 1.0×, 1.4×; Exp. 2). Results demonstrated an overall higher weighting of proprioception over vision. These weights were scaled, however, as a function of which sensory input provided more stable information across trials. Specifically, when visual gain was constantly manipulated, proprioceptive weights were higher than when proprioceptive gain was constantly manipulated. These results therefore reveal interesting characteristics of cue-weighting within the context of unfolding spatio-temporal cue dynamics.

Stance width changes how sensory feedback is used for multisegmental balance control.

A multilink sensorimotor integration model of frontal plane balance control was developed to determine how stance width influences the use of sensory feedback in healthy adults. Data used to estimate model parameters came from seven human participants who stood on a continuously rotating surface with three different stimulus amplitudes, with eyes open and closed, and at four different stance widths. Dependent variables included lower body (LB) and upper body (UB) sway quantified by frequency-response functions. Results showed that stance width had a major influence on how parameters varied across stimulus amplitude and between visual conditions. Active mechanisms dominated LB control. At narrower stances, with increasing stimulus amplitude, subjects used sensory reweighting to shift reliance from proprioceptive cues to vestibular and/or visual cues that oriented the LB more toward upright. When vision was available, subjects reduced reliance on proprioception and increased reliance on vision. At wider stances, LB control did not exhibit sensory reweighting. In the UB system, both active and passive mechanisms contributed and were dependent on stance width. UB control changed across stimulus amplitude most in wide stance (opposite of the pattern found in LB control). The strong influence of stance width on sensory integration and neural feedback control implies that rehabilitative therapies for balance disorders can target different aspects of balance control by using different stance widths. Rehabilitative strategies designed to assess or modify sensory reweighting will be most effective with the use of narrower stances, whereas wider stances present greater challenges to UB control.

Multiloop Pilot Model for Boundary-Triggered Pilot-Induced Oscillation Investigations

This paper presents the development of a multiloop pilot model for use in boundary-triggered pilot-induced oscillation investigations. In doing so, the point-tracking and boundary-avoidance elements of the pilot control strategy are assumed to act simultaneously for a point-tracking-dominant task during a boundary-avoidance tracking event. The theoretical analysis indicates that the essence of the boundary-avoidance tracking phenomenon consists of an additional requirement for the pilot to provide lead equalization as the boundary is approached as the task transitions from a full-attention point-tracking task to both a point-tracking and boundary-avoidance task. This process leads to a narrower open-loop system bandwidth and a larger tracking error, or the triggering of a pilot-induced oscillation. It is also found that the severity of the boundary-avoidance influence can be reduced by including the effects of vestibular and proprioceptive cues into the model. The boundary-avoidance tracking pilot model exhibits pilot–vehicle responses that are consistent with those observed in a piloted-simulation study and can therefore be considered to be representative of pilot activity. Consideration of the results in the round indicates that the boundary-triggered pilot-induced oscillation can be categorized as Category III pilot-induced oscillation within the existing recognized taxonomy.

Visual field dependence as a navigational strategy.

Visual perception is an important component of environmental navigation. Previous research has revealed large individual differences in navigational strategies (i.e., the body's kinesthetic and embodied approach to movement) and the perception of environmental surfaces (via distance estimations), but little research has investigated the potential relationship between these sources of individual variation. An important navigational strategy is the interaction between reliance on visual cues and vestibular or proprioceptive cues. We investigated the role of this navigational strategy in the perception of environmental surfaces. The results supported three embodied evolutionary predictions: Individuals who were most reliant on visual context (1) overestimated vertical surfaces significantly more, and (2) feared falling significantly more, than did those who were least reliant on visual context; and (3) all individuals had roughly accurate horizontal distance estimates, regardless of their navigational strategy. These are among the first data to suggest that individual differences in perception are closely related to the individual differences in navigation that derive from navigational risks. Variable navigational strategies may reflect variable capacities to perceive and navigate the environment.

Seeing by touch: evaluation of a soft biologically-inspired artificial fingertip in real-time active touch.

Effective tactile sensing for artificial platforms remains an open issue in robotics. This study investigates the performance of a soft biologically-inspired artificial fingertip in active exploration tasks. The fingertip sensor replicates the mechanisms within human skin and offers a robust solution that can be used both for tactile sensing and gripping/manipulating objects. The softness of the optical sensor's contact surface also allows safer interactions with objects. High-level tactile features such as edges are extrapolated from the sensor's output and the information is used to generate a tactile image. The work presented in this paper aims to investigate and evaluate this artificial fingertip for 2D shape reconstruction. The sensor was mounted on a robot arm to allow autonomous exploration of different objects. The sensor and a number of human participants were then tested for their abilities to track the raised perimeters of different planar objects and compared. By observing the technique and accuracy of the human subjects, simple but effective parameters were determined in order to evaluate the artificial system's performance. The results prove the capability of the sensor in such active exploration tasks, with a comparable performance to the human subjects despite it using tactile data alone whereas the human participants were also able to use proprioceptive cues.