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Neuron Nov 2018Animals rely on an internal sense of body position and movement to effectively control motor behavior. This sense of proprioception is mediated by diverse populations of...
Animals rely on an internal sense of body position and movement to effectively control motor behavior. This sense of proprioception is mediated by diverse populations of mechanosensory neurons distributed throughout the body. Here, we investigate neural coding of leg proprioception in Drosophila, using in vivo two-photon calcium imaging of proprioceptive sensory neurons during controlled movements of the fly tibia. We found that the axons of leg proprioceptors are organized into distinct functional projections that contain topographic representations of specific kinematic features. Using subclass-specific genetic driver lines, we show that one group of axons encodes tibia position (flexion/extension), another encodes movement direction, and a third encodes bidirectional movement and vibration frequency. Overall, our findings reveal how proprioceptive stimuli from a single leg joint are encoded by a diverse population of sensory neurons, and provide a framework for understanding how proprioceptive feedback signals are used by motor circuits to coordinate the body.
Topics: Animals; Drosophila melanogaster; Female; Lower Extremity; Proprioception; Sensory Receptor Cells
PubMed: 30293823
DOI: 10.1016/j.neuron.2018.09.009 -
Journal of Neuroengineering and... May 2021Neurotraumas or neurodegenerative diseases often result in proprioceptive deficits, which makes it challenging for the nervous system to adapt to the compromised... (Clinical Trial)
Clinical Trial
BACKGROUND
Neurotraumas or neurodegenerative diseases often result in proprioceptive deficits, which makes it challenging for the nervous system to adapt to the compromised sensorimotor conditions. Also, in human machine interactions, such as prosthesis control and teleoperation, proprioceptive mismatch limits accuracy and intuitiveness of controlling active joints in robotic agents. To address these proprioceptive deficits, several invasive and non-invasive approaches like vibration, electrical nerve stimulation, and skin stretch have been introduced. However, proprioceptive modulation is still challenging as the current solutions have limitations in terms of effectiveness, usability, and consistency. In this paper, we propose a new way of modulating proprioception using transcutaneous electrical stimulation. We hypothesized that transcutaneous electrical stimulation on elbow flexor muscles will induce illusion of elbow joint extension.
METHOD
Eight healthy human subjects participated in the study to test the hypothesis. Transcutaneous electrodes were placed on different locations targeting elbow flexor muscles on human subjects and experiments were conducted to identify the best locations for electrode placement, and best electrical stimulation parameters, to maximize induced proprioceptive effect. Arm matching experiments and Pinocchio illusion test were performed for quantitative and qualitative analysis of the observed effects. One-way repeated ANOVA test was performed on the data collected in arm matching experiment for statistical analysis.
RESULTS
We identified the best location for transcutaneous electrodes to induce the proprioceptive illusion, as one electrode on the muscle belly of biceps brachii short head and the other on the distal myotendinous junction of brachioradialis. The results for arm-matching and Pinocchio illusion tests showed that transcutaneous electrical stimulation using identified electrode location and electrical stimulation parameters evoked the illusion of elbow joint extension for all eight subjects, which supports our hypothesis. On average, subjects reported 6.81° angular illusion of elbow joint extension in arm-matching tests and nose elongated to 1.78 × height in Pinocchio illusion test.
CONCLUSIONS
Transcutaneous electrical stimulation, applied between the the synergistic elbow flexor muscles, consistently modulated elbow joint proprioception with the illusion of elbow joint extension, which has immense potential to be translated into various real-world applications, including neuroprosthesis, rehabilitation, teleoperation, mixed reality, and etc.
Topics: Adult; Elbow Joint; Female; Humans; Illusions; Male; Movement; Muscle, Skeletal; Proprioception; Transcutaneous Electric Nerve Stimulation
PubMed: 33941209
DOI: 10.1186/s12984-021-00870-y -
ELife Aug 2022Multiple learning processes contribute to successful goal-directed actions in the face of changing physiological states, biomechanical constraints, and environmental...
Multiple learning processes contribute to successful goal-directed actions in the face of changing physiological states, biomechanical constraints, and environmental contexts. Amongst these processes, implicit sensorimotor adaptation is of primary importance, ensuring that movements remain well-calibrated and accurate. A large body of work on reaching movements has emphasized how adaptation centers on an iterative process designed to minimize visual errors. The role of proprioception has been largely neglected, thought to play a passive role in which proprioception is affected by the visual error but does not directly contribute to adaptation. Here, we present an alternative to this visuo-centric framework, outlining a model in which implicit adaptation acts to minimize a proprioceptive error, the distance between the perceived hand position and its intended goal. This proprioceptive re-alignment model (PReMo) is consistent with many phenomena that have previously been interpreted in terms of learning from visual errors, and offers a parsimonious account of numerous unexplained phenomena. Cognizant that the evidence for PReMo rests on correlational studies, we highlight core predictions to be tested in future experiments, as well as note potential challenges for a proprioceptive-based perspective on implicit adaptation.
Topics: Adaptation, Physiological; Feedback, Sensory; Movement; Proprioception; Psychomotor Performance; Visual Perception
PubMed: 35969491
DOI: 10.7554/eLife.76639 -
International Journal of Sports... Jan 2017To determine the effect of cold ambient conditions on proprioception and cognitive function in elite alpine skiers.
PURPOSE
To determine the effect of cold ambient conditions on proprioception and cognitive function in elite alpine skiers.
METHODS
22 high-level alpine skiers and 14 control participants performed a proprioceptive-acuity (active movement-extent discrimination) and a cognitive (planning task) test in cold (8°C) and temperate (24°C) ambient conditions.
RESULTS
All participants displayed an increase in thermal discomfort and the amount of negative affects in the cold environment (all P < .05). Average proprioceptive acuity was significantly better in the elite skiers (0.46° ± 0.12°) than in the control group (0.55° ± 0.12°) (P < .05) and was not affected by cold ambient conditions, except for a shift in the pattern of error (over- vs underestimation, P < .05). Cognitive performance was similar between elite skiers and control participants in temperate environments but decreased in the cold in the control group only (P < .05) becoming lower than in elite skiers (P < .05).
CONCLUSION
Elite alpine skiers showed a significantly better proprioceptive acuity than a control population and were able to maintain their performance during a cognitive task in a cold environment.
Topics: Adult; Cognition; Cold Temperature; Humans; Male; Movement; Proprioception; Skiing; Skin Temperature; Thermosensing; Young Adult
PubMed: 27080805
DOI: 10.1123/ijspp.2016-0002 -
PLoS Biology Oct 2021Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to...
Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral nervous system cancels reafference to protect sensors and the central nervous system from being fatigued and overwhelmed by self-generated feedback. However, cancellation also limits the feedback that contributes to an animal's awareness of its body position and motion within the environment, the sense of proprioception. We propose that, rather than cancellation, CD to the fish lateral line organ restructures reafference to maximize proprioceptive information content. Fishes' undulatory body motions induce reafferent feedback that can encode the body's instantaneous configuration with respect to fluid flows. We combined experimental and computational analyses of swimming biomechanics and hair cell physiology to develop a neuromechanical model of how fish can track peak body curvature, a key signature of axial undulatory locomotion. Without CD, this computation would be challenged by sensory adaptation, typified by decaying sensitivity and phase distortions with respect to an input stimulus. We find that CD interacts synergistically with sensor polarization to sharpen sensitivity along sensors' preferred axes. The sharpening of sensitivity regulates spiking to a narrow interval coinciding with peak reafferent stimulation, which prevents adaptation and homogenizes the otherwise variable sensor output. Our integrative model reveals a vital role of CD for ensuring precise proprioceptive feedback during undulatory locomotion, which we term external proprioception.
Topics: Action Potentials; Adaptation, Physiological; Animals; Biomechanical Phenomena; Feedback, Sensory; Lateral Line System; Models, Biological; Proprioception; Swimming; Time Factors; Zebrafish
PubMed: 34634044
DOI: 10.1371/journal.pbio.3001420 -
Journal of Rehabilitation Medicine Jan 2006To evaluate whether patients suffering from whiplash-associated disorders have impaired shoulder proprioception and whether the acuity of shoulder proprioception is...
OBJECTIVE
To evaluate whether patients suffering from whiplash-associated disorders have impaired shoulder proprioception and whether the acuity of shoulder proprioception is reflected in the patients' symptoms and self-rated function.
DESIGN
A comparative group design, including a correlation design for the patient group.
SUBJECTS
Patients with chronic whiplash-associated disorders (n=37) and healthy subjects (n=41). The groups were matched for age and gender.
METHODS
All subjects underwent a shoulder proprioception test involving active ipsilateral arm position-matching. Group difference was evaluated by multiple analysis of variance and analysis of variance. The patient group completed questionnaires addressing functioning and health and performed pain ratings. Associations between proprioceptive acuity and self-rated functioning and symptoms were studied by correlation and regression analyses.
RESULTS
The patient group showed significantly lower acuity of shoulder proprioception. Moderate correlations were found between proprioceptive acuity and questionnaire scores representing physical functioning, so that low proprioceptive acuity was associated with low self-rated physical functioning. Scores representing pain-intensity did not correlate with proprioceptive acuity.
CONCLUSION
The results show that, at the group level, patients with whiplash-associated disorders have impaired shoulder proprioception. The clinical relevance of this finding is strongly supported by the association between shoulder proprioceptive acuity and self-rated functioning in the patient group.
Topics: Adult; Female; Humans; Male; Neck Pain; Pain Measurement; Posture; Predictive Value of Tests; Prognosis; Proprioception; Range of Motion, Articular; Recovery of Function; Shoulder Joint; Surveys and Questionnaires; Whiplash Injuries
PubMed: 16548086
DOI: 10.1080/16501970510042847 -
Medical Science Monitor : International... Jan 2018BACKGROUND The anterior cruciate ligament (ACL) is one of the most important structures maintaining stability of knee joints, and the proprioception of the ACL plays a...
BACKGROUND The anterior cruciate ligament (ACL) is one of the most important structures maintaining stability of knee joints, and the proprioception of the ACL plays a key role in it. If the ACL is injured in the unilateral knee joint, it changes nerve electrophysiology, morphology, and quantity of the proprioceptors in the bilateral ACL. The aim of this study was to explore the proprioceptive changes in the bilateral knee joints following unilateral ACL injury, and to provide a theoretical foundation and ideas for clinical treatment. MATERIAL AND METHODS Nine normal cynomolgus monkeys were chosen and used to developed a model of unilateral ACL injury, and 3 monkeys without modeling were used as blank control. At the 4th, 8th, and 12th weeks, the changes in ACL nerves were inspected using electrophysiology [somatosensory evoked potentials (SEPs) and motor nerve conduction velocity (MCV)], and the changes of morphology and quantity of the proprioceptors in ACL were observed and measured under gold chloride staining. RESULTS On the injured and contralateral knee joints, the incubations were extended and the amplitudes were decreased over time. In addition, with the extension of time, the total number of proprioceptors in the ACL decreased, and the variable number of proprioceptors in the ACL increased. CONCLUSIONS ACL injury leads to attenuation of proprioception on the injured side, and also leads to the attenuation of proprioception on the contralateral side, and there is a tendency could get worse over time.
Topics: Animals; Anterior Cruciate Ligament Injuries; Electrophysiological Phenomena; Evoked Potentials, Somatosensory; Knee Joint; Macaca fascicularis; Male; Neural Conduction; Proprioception
PubMed: 29305572
DOI: 10.12659/msm.905160 -
Annual International Conference of the... Nov 2021Proprioceptive deficits are common after a stroke and are thought to negatively impact motor learning. Despite this, there is a lack of practical robotic devices for... (Randomized Controlled Trial)
Randomized Controlled Trial
Proprioceptive deficits are common after a stroke and are thought to negatively impact motor learning. Despite this, there is a lack of practical robotic devices for assessing proprioception, as well as few robotic rehabilitation techniques that intensely and engagingly target proprioception. This work first presents the design of a simple robotic device, PINKIE, developed to assess and train finger proprioception. PINKIE uses low-cost actuators and sensors and is fabricated completely from 3D printed, laser cut, and off-the-shelf components. We then describe the design and testing of a gamified proprioceptive training technique, Proprioceptive-Pong (P-Pong), implemented with PINKIE. In P-Pong, players must continuously make game decisions based on sensed index and middle finger positions, as the game robotically moves their fingers instead of screen pixels to express the motion of the ball and paddle. We also report the results of a pilot study in which we investigated the effect of a short bout of P-Pong play on proprioceptive acuity, and quantified user engagement and intrinsic motivation of game play. We randomly assigned 15 unimpaired human participants to play 15 minutes of P-Pong (proprioceptive training group) or a similar but video-only version of Pong (control group). We assessed finger proprioception acuity before and after game play using the Crisscross assessment previously developed by our laboratory, engagement using the User Engagement Scale, and motivation using the Intrinsic Motivation Inventory survey. Following game play, there was a significant improvement in proprioceptive acuity (2.2 ± 2.6 SD mm, p = 0.023) in the proprioceptive training group but not the control group (0.5 ± 0.9 SD mm, p = 0.101). Participants rated P-Pong highly on all survey subscales, and as highly as visual Pong, except in the Perceived Usability and Competence subscales, a finding we discuss. To our knowledge, this work presents the first computer gaming approach for providing intense and engaging finger proprioception training, by splitting the feedback of game elements between the visual and proprioceptive senses. The pilot experiment indicates that the human sensory motor system has the ability to at least temporarily improve proprioception acuity with such game-based training.
Topics: Fingers; Humans; Pilot Projects; Proprioception; Robotics; Video Games
PubMed: 34892649
DOI: 10.1109/EMBC46164.2021.9631041 -
The Journal of Physiology Dec 2022Robust locomotion relies on information from proprioceptors: sensory organs that communicate the position of body parts to the spinal cord and brain. Proprioceptive...
Robust locomotion relies on information from proprioceptors: sensory organs that communicate the position of body parts to the spinal cord and brain. Proprioceptive circuits in the spinal cord are known to coarsely regulate locomotion in the presence of perturbations. Yet, the regulatory importance of the brain in maintaining robust locomotion remains less clear. Here, through mouse genetic studies and in vivo electrophysiology, we examined the role of the brain in integrating proprioceptive information during perturbed locomotion. The systemic removal of proprioceptors left the mice in a constantly perturbed state, similar to that observed during mechanically perturbed locomotion in wild-type mice and characterised by longer and less accurate synergistic activation patterns. By contrast, after surgically interrupting the ascending proprioceptive projection to the brain through the dorsal column of the spinal cord, wild-type mice showed normal walking behaviour, yet lost the ability to respond to external perturbations. Our findings provide direct evidence of a pivotal role for ascending proprioceptive information in achieving robust, safe locomotion. KEY POINTS: Whether brain integration of proprioceptive feedback is crucial for coping with perturbed locomotion is not clear. We showed a crucial role of the brain for responding to external perturbations and ensure robust locomotion. We used mouse genetics to remove proprioceptors and a spinal lesion model to interrupt the flow of proprioceptive information to the brain through the dorsal column in wild-type animals. Using a custom-built treadmill, we administered sudden and random mechanical perturbations to mice during walking. External perturbations affected locomotion in wild-type mice similar to the absence of proprioceptors in genetically modified mice. Proprioceptive feedback from muscle spindles and Golgi tendon organs contributed to locomotor robustness. Wild-type mice lost the ability to respond to external perturbations after interruption of the ascending proprioceptive projection to the brainstem.
Topics: Animals; Mice; Proprioception; Locomotion; Muscle Spindles; Feedback, Sensory; Brain
PubMed: 36271747
DOI: 10.1113/JP283181 -
ELife Oct 2022The voltage-gated sodium channel (Na), Na1.1, is well-studied in the central nervous system; conversely, its contribution to peripheral sensory neuron function is more...
The voltage-gated sodium channel (Na), Na1.1, is well-studied in the central nervous system; conversely, its contribution to peripheral sensory neuron function is more enigmatic. Here, we identify a new role for Na1.1 in mammalian proprioception. RNAscope analysis and in vitro patch-clamp recordings in genetically identified mouse proprioceptors show ubiquitous channel expression and significant contributions to intrinsic excitability. Notably, genetic deletion of Na1.1 in sensory neurons caused profound and visible motor coordination deficits in conditional knockout mice of both sexes, similar to conditional Piezo2-knockout animals, suggesting that this channel is a major contributor to sensory proprioceptive transmission. Ex vivo muscle afferent recordings from conditional knockout mice found that loss of Na1.1 leads to inconsistent and unreliable proprioceptor firing characterized by action potential failures during static muscle stretch; conversely, afferent responses to dynamic vibrations were unaffected. This suggests that while a combination of Piezo2 and other Na isoforms is sufficient to elicit activity in response to transient stimuli, Na1.1 is required for transmission of receptor potentials generated during sustained muscle stretch. Impressively, recordings from afferents of heterozygous conditional knockout animals were similarly impaired, and heterozygous conditional knockout mice also exhibited motor behavioral deficits. Thus, Na1.1 haploinsufficiency in sensory neurons impairs both proprioceptor function and motor behaviors. Importantly, human patients harboring Na1.1 loss-of-function mutations often present with motor delays and ataxia; therefore, our data suggest that sensory neuron dysfunction contributes to the clinical manifestations of neurological disorders in which Na1.1 function is compromised. Collectively, we present the first evidence that Na1.1 is essential for mammalian proprioceptive signaling and behaviors.
Topics: Animals; Female; Humans; Male; Mice; Action Potentials; Mice, Knockout; Proprioception; Sensory Receptor Cells; NAV1.1 Voltage-Gated Sodium Channel
PubMed: 36278870
DOI: 10.7554/eLife.79917