The proprioceptive map of the arm is systematic and stable, but idiosyncratic

Visual and somatosensory signals participate together in providing an estimate of the hand's spatial location. While the ability of subjects to identify the spatial location of their hand based on visual and proprioceptive signals has previously been characterized, relatively few studies have examined in detail the spatial structure of the proprioceptive map of the arm. Here, we reconstructed and analyzed the spatial structure of the estimation errors that resulted when subjects reported the location of their unseen hand across a 2D horizontal workspace. Hand position estimation was mapped under four conditions: with and without tactile feedback, and with the right and left hands. In the task, we moved each subject's hand to one of 100 targets in the workspace while their eyes were closed. Then, we either a) applied tactile stimulation to the fingertip by allowing the index finger to touch the target or b) as a control, hovered the fingertip 2 cm above the target. After returning the hand to a neutral position, subjects opened their eyes to verbally report where their fingertip had been. We measured and analyzed both the direction and magnitude of the resulting estimation errors. Tactile feedback reduced the magnitude of these estimation errors, but did not change their overall structure. In addition, the spatial structure of these errors was idiosyncratic: each subject had a unique pattern of errors that was stable between hands and over time. Finally, we found that at the population level the magnitude of the estimation errors had a characteristic distribution over the workspace: errors were smallest closer to the body. The stability of estimation errors across conditions and time suggests the brain constructs a proprioceptive map that is reliable, even if it is not necessarily accurate. The idiosyncrasy across subjects emphasizes that each individual constructs a map that is unique to their own experiences.     

Bodily Illusions in Young Children: Developmental Change in Visual and Proprioceptive Contributions to Perceived Hand Position

We examined the visual capture of perceived hand position in forty-five 5- to 7-year-olds and in fifteen young adults, using a mirror illusion task. In this task, participants see their left hand on both the left and right (by virtue of a mirror placed at the midline facing the left arm, and obscuring the right). The accuracy of participants’ reaching was measured when proprioceptive and visual cues to the location of the right arm were put into conflict (by placing the arms at different distances from the mirror), and also when only proprioceptive information was available (i.e., when the mirror was covered). Children in all age-groups (and adults) made reaching errors in the mirror condition in accordance with the visually-specified illusory starting position of their hand indicating a visual capture of perceived hand position. Data analysis indicated that visual capture increased substantially up until 6 years of age. These findings are interpreted with respect to the development of the visual guidance of action in early childhood.     

Correlation analysis of proprioceptive acuity in ipsilateral position-matching and velocity-discrimination

In order to plan and control movements the central nervous system (CNS) needs to continuously keep track of the state of the musculoskeletal system. Therefore the CNS constantly uses sensory input from mechanoreceptors in muscles, joints and skin to update information about body configuration on different levels of the CNS. On the conscious level, such representations constitute proprioception. Different tests for assessment of proprioceptive acuity have been described. However, it is unclear if the proprioceptive acuity measurements in these tests correlate within subjects. By using both uni- and multivariate analysis we compared proprioceptive acuity in different variants of ipsilateral active and passive limb position-matching and ipsilateral passive limb movement velocity-discrimination in a group of healthy subjects. The analysis of the position-matching data revealed a higher acuity of matching for active movements in comparison to passive ones. The acuity of matching was negatively correlated to movement extent. There was a lack of correlation between proprioceptive acuity measurements in position-matching and velocity-discrimination.     

Correlation analysis of proprioceptive acuity in ipsilateral position-matching and velocity-discrimination

In order to plan and control movements the central nervous system (CNS) needs to continuously keep track of the state of the musculoskeletal system. Therefore the CNS constantly uses sensory input from mechanoreceptors in muscles, joints and skin to update information about body configuration on different levels of the CNS. On the conscious level, such representations constitute proprioception. Different tests for assessment of proprioceptive acuity have been described. However, it is unclear if the proprioceptive acuity measurements in these tests correlate within subjects. By using both uni- and multivariate analysis we compared proprioceptive acuity in different variants of ipsilateral active and passive limb position-matching and ipsilateral passive limb movement velocity-discrimination in a group of healthy subjects. The analysis of the position-matching data revealed a higher acuity of matching for active movements in comparison to passive ones. The acuity of matching was negatively correlated to movement extent. There was a lack of correlation between proprioceptive acuity measurements in position-matching and velocity-discrimination.     

Proprioceptive Interaction between the Two Arms in a Single-Arm Pointing Task

Proprioceptive signals coming from both arms are used to determine the perceived position of one arm in a two-arm matching task. Here, we examined whether the perceived position of one arm is affected by proprioceptive signals from the other arm in a one-arm pointing task in which participants specified the perceived position of an unseen reference arm with an indicator paddle. Both arms were hidden from the participant’s view throughout the study. In Experiment 1, with both arms placed in front of the body, the participants received 70–80 Hz vibration to the elbow flexors of the reference arm (= right arm) to induce the illusion of elbow extension. This extension illusion was compared with that when the left arm elbow flexors were vibrated or not. The degree of the vibration-induced extension illusion of the right arm was reduced in the presence of left arm vibration. In Experiment 2, we found that this kinesthetic interaction between the two arms did not occur when the left arm was vibrated in an abducted position. In Experiment 3, the vibration-induced extension illusion of one arm was fully developed when this arm was placed at an abducted position, indicating that the brain receives increased proprioceptive input from a vibrated arm even if the arm was abducted. Our results suggest that proprioceptive interaction between the two arms occurs in a one-arm pointing task when the two arms are aligned with one another. The position sense of one arm measured using a pointer appears to include the influences of incoming information from the other arm when both arms were placed in front of the body and parallel to one another.     

Where is my hand in space? The internal model of gravity influences proprioception

Knowing where our limbs are in space is crucial for a successful interaction with the external world. Joint position sense (JPS) relies on both cues from muscle spindles and joint mechanoreceptors, as well as the effort required to move. However, JPS may also rely on the perceived external force on the limb, such as the gravitational field. It is well known that the internal model of gravity plays a large role in perception and behaviour. Thus, we have explored whether direct vestibular-gravitational cues could influence JPS. Participants passively estimated the position of their hand while they were upright and therefore aligned with terrestrial gravity, or pitch-tilted 45° backwards from gravity. Overall participants overestimated the position of their hand in both upright and tilted postures; however, the proprioceptive bias was significantly reduced when participants were tilted. Our findings therefore suggest that the internal model of gravity may influence and update JPS in order to allow the organism to interact with the environment.     

Proprioception,the regulator of motor function

In animals, proper locomotion is crucial to find mates and foods and avoid predators or dangers. Multiple sensory systems detect external and internal cues and integrate them to modulate motor outputs. Proprioception is the internal sense of body position, and proprioceptive control of locomotion is essential to generate and maintain precise patterns of movement or gaits. This proprioceptive feedback system is conserved in many animal species and is mediated by stretch-sensitive receptors called proprioceptors. Recent studies have identified multiple proprioceptive neurons and proprioceptors and their roles in the locomotion of various model organisms. In this review we describe molecular and neuronal mechanisms underlying proprioceptive feedback systems in C. elegans, Drosophila, and mice.     

Links between vision and somatosensation. Vision can improve the felt position of the unseen hand.

During reaching movements, sensory signals must be transformed into appropriate motor commands. Anatomical, electrophysiological, and neuropsychological evidence suggest that there is no single, supramodal map of space that is used to guide reaching. Instead, movements appear to be planned and controlled within multiple coordinate systems, each one attached to a different body part. Recent neuropsychological investigations demonstrating that somatosensory impairments can be ameliorated by visual cues, and visual impairments by proprioceptive cues, have been interpreted as evidence that arm-centered representations may exist in humans. A critical difference between the findings obtained in the monkey and in humans, however, is that in the latter case, vision of the limb appears be critical for visual somatosensory binding. Here, we report a case study of a patient (C.T.) recovering from unilateral somatosensory impairment, including tactile extinction, who executed reaches toward visually defined or proprioceptively defined locations. We demonstrate that when the target location of a reach was defined proprioceptively, by passively positioning our patient's impaired hand beneath the table surface, vision of the workspace immediately adjacent to the unseen hand dramatically increased the endpoint accuracy of her reaching movements, even though such cues could not possibly signal the position of the target directly.     

Effects of Modulations of the Visual Conditions on Subjects’ Perception of Their Own and Another Person’s Hand

According to current concepts, the execution of expedient actions well-coordinated in space becomes possible owing to the creation of a system for internal representation, which includes a body coordinate system, in the central nervous system. The goal of this study was to assess the effects induced by the exclusion of vision and a left-right inversion in visual space on the accuracy in the internal representation of hands and on aimed arm movements. The study cohort included 16 participants aged from 18 to 25 years. The experiment consisted of two test series. In the first series, a subject placed his/her left hand under a transparent plexiglass screen. Upon the experimenter’s command, the subject had to indicate the position of his/her left wrist and the terminal phalanges of the thumb, middle and little fingers with his/her right index finger on the plexiglass, which was accompanied by the corresponding marks displayed on the screen. The positional accuracy in the subject’s perception of his/her own hand position was recorded in the conditions of a leftright inversion of visual space, which were created by wearing prismatic spectacles and the exclusion of visual control. In the second case, the subject’s left hand was replaced on the table under the transparent screen by a similarly shaped left hand belonging to another person. It has been shown that the positions of the middle fingertip and the wrist were sufficiently precisely perceived by the subject through prismatic spectacles. However, the position of the tips of the thumb and little finger relative to the axis connecting the wrist and the terminal phalanx of the middle finger (the hand axis) was perceptually inverted. The accuracy of the indication was reduced for all fingers when the eyes were closed. In testing another person’s hand, a left–right inversion in the visual space created an illusory 90° turn of the hand’s axis and an illusory bias relative to the wrist towards elongation in the marker points corresponding to another person’s fingers. We can suggest that when the alien hand replaced the subject’s own hand, in accordance with the modulations in the motor task conditions, the egocentric system of coordinates was replaced by the allocentric system. The role of vision in the execution of spatially oriented and accurate hand movements increased in this case.     

A neural network model for the intersensory coordination involved in goal-directed movements

A neural network model for a sensorimotor system, which was developed to simulate oriented movements in man, is presented. It is composed of a formal neural network comprising two layers: a sensory layer receiving and processing sensory inputs, and a motor layer driving a simulated arm. The sensory layer is an extension of the topological network previously proposed by Kohonen (1984). Two kinds of sensory modality, proprioceptive and exteroceptive, are used to define the arm position. Each sensory cell receives proprioceptive inputs provided by each arm-joint together with the exteroceptive inputs. This sensory layer is therefore a kind of associative layer which integrates two separate sensory signals relating to movement coding. It is connected to the motor layer by means of adaptive synapses which provide a physical link between a motor activity and its sensory consequences. After a learning period, the spatial map which emerges in the sensory layer clearly depends on the sensory inputs and an associative map of both the arm and the extra-personal space is built up if proprioceptive and exteroceptive signals are processed together. The sensorimotor transformations occuring in the junctions linking the sensory and motor layers are organized in such a manner that the simulated arm becomes able to reach towards and track a target in extra-personal space. Proprioception serves to determine the final arm posture adopted and to correct the ongoing movement in cases where changes in the target location occur. With a view to developing a sensorimotor control system with more realistic salient features, a robotic model was coupled with the formal neural network. This robotic implementation of our model shows the capacity of formal neural networks to control the displacement of mechanical devices.     

Differential Contributions of Vision,Touch and Muscle Proprioception to the Coding of Hand Movements

To further elucidate the mechanisms underlying multisensory integration, this study examines the controversial issue of whether congruent inputs from three different sensory sources can enhance the perception of hand movement. Illusory sensations of clockwise rotations of the right hand were induced by either separately or simultaneously stimulating visual, tactile and muscle proprioceptive channels at various intensity levels. For this purpose, mechanical vibrations were applied to the pollicis longus muscle group in the subjects’ wrists, and a textured disk was rotated under the palmar skin of the subjects’ right hands while a background visual scene was projected onto the rotating disk. The elicited kinaesthetic illusions were copied by the subjects in real time and the EMG activity in the adductor and abductor wrist muscles was recorded. The results show that the velocity of the perceived movements and the amplitude of the corresponding motor responses were modulated by the nature and intensity of the stimulation. Combining two sensory modalities resulted in faster movement illusions, except for the case of visuo-tactile co-stimulation. When a third sensory input was added to the bimodal combinations, the perceptual responses increased only when a muscle proprioceptive stimulation was added to a visuo-tactile combination. Otherwise, trisensory stimulation did not override bimodal conditions that already included a muscle proprioceptive stimulation. We confirmed that vision or touch alone can encode the kinematic parameters of hand movement, as is known for muscle proprioception. When these three sensory modalities are available, they contribute unequally to kinaesthesia. In addition to muscle proprioception, the complementary kinaesthetic content of visual or tactile inputs may optimize the velocity estimation of an on-going movement, whereas the redundant kinaesthetic content of the visual and tactile inputs may rather enhance the latency of the perception.     

The Rubber Hand Illusion: feeling of ownership and proprioceptive drift do not go hand in hand

In the Rubber Hand Illusion, the feeling of ownership of a rubber hand displaced from a participant's real occluded hand is evoked by synchronously stroking both hands with paintbrushes. A change of perceived finger location towards the rubber hand (proprioceptive drift) has been reported to correlate with this illusion. To measure the time course of proprioceptive drift during the Rubber Hand Illusion, we regularly interrupted stroking (performed by robot arms) to measure perceived finger location. Measurements were made by projecting a probe dot into the field of view (using a semi-transparent mirror) and asking participants if the dot is to the left or to the right of their invisible hand (Experiment 1) or to adjust the position of the dot to that of their invisible hand (Experiment 2). We varied both the measurement frequency (every 10 s, 40 s, 120 s) and the mode of stroking (synchronous, asynchronous, just vision). Surprisingly, with frequent measurements, proprioceptive drift occurs not only in the synchronous stroking condition but also in the two control conditions (asynchronous stroking, just vision). Proprioceptive drift in the synchronous stroking condition is never higher than in the just vision condition. Only continuous exposure to asynchronous stroking prevents proprioceptive drift and thus replicates the differences in drift reported in the literature. By contrast, complementary subjective ratings (questionnaire) show that the feeling of ownership requires synchronous stroking and is not present in the asynchronous stroking condition. Thus, subjective ratings and drift are dissociated. We conclude that different mechanisms of multisensory integration are responsible for proprioceptive drift and the feeling of ownership. Proprioceptive drift relies on visuoproprioceptive integration alone, a process that is inhibited by asynchronous stroking, the most common control condition in Rubber Hand Illusion experiments. This dissociation implies that conclusions about feelings of ownership cannot be drawn from measuring proprioceptive drift alone.     

Haptic perception of object curvature in Parkinson's disease

Background

The haptic perception of the curvature of an object is essential for adequate object manipulation and critical for our guidance of actions. This study investigated how the ability to perceive the curvature of an object is altered by Parkinson''s disease (PD).

Methodology/Principal Findings

Eight healthy subjects and 11 patients with mild to moderate PD had to judge, without vision, the curvature of a virtual “box” created by a robotic manipulandum. Their hands were either moved passively along a defined curved path or they actively explored the curved curvature of a virtual wall. The curvature was either concave or convex (bulging to the left or right) and was judged in two locations of the hand workspace–a left workspace location, where the curved hand path was associated with curved shoulder and elbow joint paths, and a right workspace location in which these joint paths were nearly linear. After exploring the curvature of the virtual object, subjects had to judge whether the curvature was concave or convex. Based on these data, thresholds for curvature sensitivity were established. The main findings of the study are: First, 9 out 11 PD patients (82%) showed elevated thresholds for detecting convex curvatures in at least one test condition. The respective median threshold for the PD group was increased by 343% when compared to the control group. Second, when distal hand paths became less associated with proximal joint paths (right workspace), haptic acuity was reduced substantially in both groups. Third, sensitivity to hand trajectory curvature was not improved during active exploration in either group.

Conclusion/Significance

Our data demonstrate that PD is associated with a decreased acuity of the haptic sense, which may occur already at an early stage of the disease.     

Patterns of spinal sensory-motor connectivity prescribed by a dorsoventral positional template

Sensory-motor circuits in the spinal cord are constructed with a fine specificity that coordinates motor behavior, but the mechanisms that direct sensory connections with their motor neuron partners remain unclear. The dorsoventral settling position of motor pools in the spinal cord is known to match the distal-to-proximal position of their muscle targets in the limb, but the significance of invariant motor neuron positioning is unknown. An analysis of sensory-motor connectivity patterns in FoxP1 mutant mice, where motor neuron position has been scrambled, shows that the final pattern of sensory-motor connections is initiated by the projection of sensory axons to discrete dorsoventral domains of the spinal cord without regard for motor neuron subtype or, indeed, the presence of motor neurons. By implication, the clustering and dorsoventral settling position of motor neuron pools serve as a determinant of the pattern of sensory input specificity and thus motor coordination.     

Vibration of neck muscles changes the apparent position of a visual target

The discharge rate of muscle spindle afferents normally provides a precise signal of muscle length. Vibration of a muscle or its tendon induces an increase in afferent discharge which then no longer represents true muscle length; however, this increased proprioceptive input is interpreted in the central nervous system as a lengthening of the muscle. The incremented signal gives rise to illusions of displacement, or movement, of a fixed, vibrated limb. A visual target attached to such a vibrated limb also appears to move. We now report that vibration of the neck muscles influences visual localisation by inducing illusory movement of targets in visual space. Subjects were seated in a totally dark room and viewed a light-emitting diode (LED). The LED was placed at eye level approximately in the body midline at a distance of 70 cm. They held a physiotherapy vibrator in the left hand with its tip against the left side of the neck. When vibration was initiated the LED appeared to move rightward. The position of the tip of the vibrator was adjusted to produce the maximum apparent displacement to the right. In some subjects the illusion had a vertical component. Subjects maintained the vibrator in position and described the illusion when vibration began, during vibration and at its end. They reported that, initially, the target moved to the right but this displacement ceased after a second or two. The target then appeared to continue in motion without changing its position. When vibration ended the target returned to its initial position.(ABSTRACT TRUNCATED AT 250 WORDS)     

Spatial code interference on directional responses.

The interference from an irrelevant position cue was compared in a reaction-time paradigm using voice and manual responses. The subjects were required to say 'left' or 'right' or to press left or right keys in response to arrow directions, and the arrows were presented at left or right side display positions irrelevant to the task. Display position significantly increased latency when it did not match the response to the relevant direction cue for both spatial (key-press) and non-spatial (voice) responses (73 and 59 ms, respectively). When presented alone, the position cue was processed faster than the direction cue for both manual and verbal responses. Results are discussed in terms of a common abstract mediator for left-right responses between modes and the processing speed difference between the relevant and irrelevant cue. The irrelevant left-right position code may occupy some limited-capacity channel ahead of the left-right code derived from processing the relevant direction cue.     

Arboreal Postures Elicit Hand Preference when Accessing a Hard-to-Reach Foraging Device in Captive Bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>)

Arboreal, and in particular suspensory, postures may elicit a preference for the strongest limb to be used in postural support in large bodied primates. However, selection may have favored ambilaterality rather than a preference for a particular hand in chimpanzees (Pan troglodytes) fishing arboreally for ants. To investigate the influence of arboreality on hand preference we recorded handedness in seven captive bonobos (Pan paniscus) manipulating a foraging device during terrestrial and arboreal postures in a symmetrical environment, observing 2726 bouts of manipulation. When accessing the foraging device in the arboreal position the bonobos adopted predominantly suspensory postures. There was no population level hand preference for manipulating the foraging device in either the terrestrial or arboreal positions. However, four of seven individuals that interacted with the foraging devices showed a significant preference for one hand (two were left handed, two were right handed) when manipulating the foraging device in the arboreal position whereas only one individual (left handed) showed a preference in the terrestrial position. This suggests that individuals may have a preferred or strongest limb for postural support in a symmetrical arboreal environment, resulting in a bias to use the opposite hand for manipulation. However, the hand that is preferred for postural support differs between individuals. Although our sample is for two captive groups at the same zoo, our findings suggest that the demand of maintaining arboreal postures and environmental complexity influence hand preference.     

Development and Application of Stereo Camera-Based Upper Extremity Workspace Evaluation in Patients with Neuromuscular Diseases

Background

The concept of reachable workspace is closely tied to upper limb joint range of motion and functional capability. Currently, no practical and cost-effective methods are available in clinical and research settings to provide arm-function evaluation using an individual’s three-dimensional (3D) reachable workspace. A method to intuitively display and effectively analyze reachable workspace would not only complement traditional upper limb functional assessments, but also provide an innovative approach to quantify and monitor upper limb function.

Methodology/Principal Findings

A simple stereo camera-based reachable workspace acquisition system combined with customized 3D workspace analysis algorithm was developed and compared against a sub-millimeter motion capture system. The stereo camera-based system was robust, with minimal loss of data points, and with the average hand trajectory error of about 40 mm, which resulted to ∼5% error of the total arm distance. As a proof-of-concept, a pilot study was undertaken with healthy individuals (n = 20) and a select group of patients with various neuromuscular diseases and varying degrees of shoulder girdle weakness (n = 9). The workspace envelope surface areas generated from the 3D hand trajectory captured by the stereo camera were compared. Normalization of acquired reachable workspace surface areas to the surface area of the unit hemi-sphere allowed comparison between subjects. The healthy group’s relative surface areas were 0.618±0.09 and 0.552±0.092 (right and left), while the surface areas for the individuals with neuromuscular diseases ranged from 0.03 and 0.09 (the most severely affected individual) to 0.62 and 0.50 (very mildly affected individual). Neuromuscular patients with severe arm weakness demonstrated movement largely limited to the ipsilateral lower quadrant of their reachable workspace.

Conclusions/Significance

The findings indicate that the proposed stereo camera-based reachable workspace analysis system is capable of distinguishing individuals with varying degrees of proximal upper limb functional impairments.     

A gain-field encoding of limb position and velocity in the internal model of arm dynamics

Adaptability of reaching movements depends on a computation in the brain that transforms sensory cues, such as those that indicate the position and velocity of the arm, into motor commands. Theoretical consideration shows that the encoding properties of neural elements implementing this transformation dictate how errors should generalize from one limb position and velocity to another. To estimate how sensory cues are encoded by these neural elements, we designed experiments that quantified spatial generalization in environments where forces depended on both position and velocity of the limb. The patterns of error generalization suggest that the neural elements that compute the transformation encode limb position and velocity in intrinsic coordinates via a gain-field; i.e., the elements have directionally dependent tuning that is modulated monotonically with limb position. The gain-field encoding makes the counterintuitive prediction of hypergeneralization: there should be growing extrapolation beyond the trained workspace. Furthermore, nonmonotonic force patterns should be more difficult to learn than monotonic ones. We confirmed these predictions experimentally.