Comprehensive Physiology Wiley Online Library

Kinesthesia: Roles for Afferent Signals and Motor Commands

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Abstract

The sections in this article are:

1 Historical Perspectives
2 Current Definitions
3 Properties of Kinesthetic Afferents
3.1 Muscle Spindles
3.2 Tendon Organ Afferents
3.3 Joint Afferents
3.4 Cutaneous Afferents
3.5 Possible Kinesthetic Role for Group III and IV Fibers
3.6 Cortical Projections
4 Kinesthetic Mechanisms in Isolation
4.1 Illusions Produced by Stimulation of Kinesthetic Afferents
4.2 Electrical Stimulation of Muscle, Joint, and Cutaneous Afferents
4.3 Sensations of Joint Position and Movement
4.4 Assessment of Movement Sensation
4.5 Senses of Force and Heaviness
4.6 Sense of Timing of Muscle Action
4.7 Other Roles for Motor Commands
5 Deafferentation
6 Functional Aspects of Kinesthesia
6.1 Body Schema
6.2 Muscle Fatigue
6.3 Altered Kinesthesia with Aging
6.4 Changes in Kinesthesia with Joint Pathology
7 Conclusions
Figure 1. Figure 1.

Schematic representation of one efference copy mechanism used by mormyrid fish. The electric organ discharges in response to the command from the electric organ discharge nucleus and this evokes a reafferent signal in the knollenorgan receptor. Environmentally mediated events evoke exafferent signals in this receptor. The efference copy acts as an exact inhibitory template to block reafferent signals so that the fish can more easily detect the environmental signals. Here, the corollary discharge provides a precise template of the expected reafference (see text).

Adapted from Bell
Figure 2. Figure 2.

Modulation of muscle spindle discharge by small length changes diminishes markedly when they are superimposed on slow movements. Data from a population of primary spindle afferents innervating the cat soleus muscle to illustrate the effects of an underlying slow movement on the sensitivity to sinusoidal stretch delivered at about 1 Hz. Panels at left show the control sinusoidal stretch (upper trace) and the sinusoidal stretch delivered during a slow “triangular” movement (lower trace). Panels at right show the responses for a 50 μm (above) and 1,000 μm sinusoid (below). Responses to combined sinusoidal and triangular stretch shown as the median (thick line) with interquartile ranges. Open circle indicates the control responses without slow movement. Sensitivity scale is enlarged in the lower panel, with the cross in the upper panel indicating the corresponding response to 1,000 μm sinusoid during the fastest movement. These results mean that primary spindle afferents will encode large changes in length faithfully but will only respond dynamically to very small perturbations when the movement is very slow or isometric.

Adapted from Baumann and Hulliger
Figure 3. Figure 3.

A, Comparison between responses of a primary muscle spindle afferent and Golgi tendon organ in the cat soleus muscle to longitudinal vibration under control conditions and during a contraction produced by intense ventral root stimulation. The primary muscle spindle ending follows 1:1 the vibration at 400 Hz (10 m) under control conditions. Its discharge increases during contraction (due to fusimotor activation), but, during combined contraction and vibration, the response is less than under control conditions. The tendon organ requires larger amplitude vibration to respond at rest (200 Hz, 150 m), increases its discharge during muscle contraction, but, during combined contraction and vibration, the response is 1:1 and greater than under the control conditions. (Adapted from Brown, Engberg, and Matthews .] B, Behavior of a Golgi tendon organ afferent to vibration applied transversely to the tibialis anterior tendon at 40 Hz when the muscle is relaxed (upper panels) and during a weak voluntary contraction (lower panels). The unit responds at a subharmonic of the vibration frequency during relaxation but responds 1:1 with vibration during the contraction.

From Roll, Vedel, and Ribot .] While it is possible that the response of the Golgi tendon organ afferents shown in these two panels represents the extreme of their behavior, nonetheless, some will behave this way under natural conditions
Figure 4. Figure 4.

Responses of ten tendon organ afferents innervating peroneus tertius muscle in the cat to motor unit forces produced by stimulation of one or two motor units. A, Average tendon organ responses to the forces from motor unit A (left panel), motor unit B (middle panel), and both motor units (right panel). Stimuli given at 10, 20, and 40 Hz. Motor unit A activated six tendon organs and motor unit B activated four tendon organs (shared with motor unit A). Average tendon organ response calculated from the responses of the activated tendon organs. When both motor units contract to 40 Hz stimulation, force at the tendon adds as expected from the algebraic sum of the force to each motor unit, but the average discharge frequency does not exceed that when unit 2 contracts alone. Note that in the right panel the average tendon organ response to stimulation of both motor units at 20 Hz is less after the tetanus at 40 Hz.

Adapted from Jami .] B, Predicted ensemble response for the data in part A of the figure when the total number of tendon organ discharges is calculated (from their average discharge and the number activated). This has been estimated for the tetani produced by 40 Hz stimuli and the two sets of 20 Hz stimuli. Total tendon organ input increases very well with tendon force
Figure 5. Figure 5.

Behavior of a joint afferent from the proximal interphalangeal joint of the index finger recorded from the median nerve. Responses during passive rotation in the flexion‐extension axis. Inset shows a tonic discharge when the joint was in the rest position. Upper trace, Instantaneous frequency. Lower trace, Goniometer record. Note the sustained high‐frequency discharge when the joint was moved into extreme extension, with no change in background discharge when it moved into flexion but a sustained discharge when forced into extreme flexion. Many receptors of this type also responded to movements in the abduction‐adduction or extorsion‐intorsion axis.

Adapted from Burke, Gandevia, and Macefield
Figure 6. Figure 6.

A, Responses of a typical SA II afferent innervating the skin on the dorsum of the hand during voluntary flexion and extension of the metacarpophalangeal joint of the index finger. B, The receptive field and response to focal indentation of the skin. Despite its “remote” location, the afferent responds to the voluntary movements.

Adapted from Edin and Abbs .] C, Summary of the responsiveness of a sample of SA II cutaneous afferents innervating the dorsum of the hand and muscle spindle afferents from extensors of the index finger to movement of the metacarpophalangeal joint of the index finger with the muscles relaxed. The three vertical axes refer to different methods of measuring the static and dynamic sensitivity of the afferents to applied movements. From Grill and Hallert
Figure 7. Figure 7.

A, Movement illusions recorded when vibrators are applied to the distal tendons of the left biceps brachii and triceps brachii. Left arm is fixed and the right (tracking arm) is mobile and connected to a goniometer. The subject matches the perceived movement during vibration of the biceps tendon at different frequencies. The speed of the illusory extension movement increases with vibration frequency but diminishes at the highest frequency, presumably because the primary spindle afferents no longer follow 1:1 the vibrator frequency.

Adapted from Roll and Vedel .] B, Superimposed data from one subject for combinations of vibration applied simultaneously to the biceps and triceps muscles. Perceived movement of the vibrated arm depends on the difference in frequencies of vibration, with an illusory movement of extension when the vibration frequency is greater for the flexors than extensors. [Adapted from Gilhodes, Roll, and Tardy‐Gervet .] C, During trains of stimuli delivered to the ulnar nerve at the wrist (below motor threshold and without inducing cutaneous paresthesias), the subject experienced illusory flexion of the interphalangeal joints and extension of the metacarpophalangeal (MCP) joint. The complex illusory motion at three joints is consistent with perceived elongation of the interosseous and lumbrical muscles acting on the ring finger. The component at the MCP joint was measured with matching movements on the contralateral side. Relationship between stimulus frequency and perceived velocity for one subject. By comparison with A, the illusory movement (mean ± SEM) increases progressively even at stimulus frequencies above 100/s. This suggests that mechanical entrainment of spindle afferent discharge is impaired at higher vibration frequencies. Reproduced from Gandevia and Gandevia and Burke
Figure 8. Figure 8.

Position‐sense thresholds for detection of joint displacements at the metacarpophalangeal (MCP), proximal interphalangeal (PIP), and distal interphalangeal (DIP) joints of the middle finger in five subjects. Movements were delivered with the joint in the midrange at 2 degrees min (i.e., below the velocity at which movement sensations occur). Each point depicts data from one subject with filled circles for control performance under passive conditions and open circles for estimates when voluntary contraction of the flexors and extensors occurred after the final position had been reached. In one condition, the hand was postured so that the distal joint of the middle finger could not be moved by voluntary contractions and thus the joint was effectively disengaged from its attachments.

Adapted from Taylor and McCloskey
Figure 9. Figure 9.

A, Detection of 5‐degree movements at different angular velocities from a midposition of the distal interphalangeal joint of the middle finger. Subjects had to nominate correctly the direction of the movement. Mean data from references 55 and 91 have been pooled. Data with the hand postured so as to disengage the flexor and extensor muscles are shown as open circles . Filled circles represent performance when the distal interphalangeal joint was injected with local anesthetic. Performance is best when the muscle, joint, and cutaneous afferents are all intact (hatched horizontal bar): it deteriorates when muscles cannot contribute to movement detection and deteriorates further when the joint space is injected with local anesthetic. (From Gandevia and Burke .] B, Distribution of modular errors for the perceived position of the proximal interphalangeal joint of the index finger under control conditions (upper panel) and when the digital nerves of the finger had been blocked with local anesthetic (lower panel).

Adapted from Ferrell and Smith .] A schematic view of the perceived position of the proximal joint of the finger during digital anesthesia shown by the dashed lines. The range of perceived positions of the joint was compressed when joint and cutaneous afferents were anesthetized. C, Schematic representation of the distortion of position sense induced by a digital nerve block
Figure 10. Figure 10.

A, Detection of the direction of movements applied to the distal interphalangeal joint of the middle finger when the digit was anesthetized at its base (open circles) and when the subject exerted a weak flexor contraction with the anesthetized finger (filled circles). The hand was postured so that only contraction of the long flexor moved the joint. Proprioceptive acuity was restored to within the normal range when muscle contraction occurred in the absence of local joint and cutaneous inputs (compare Fig. A). Remote cutaneous signals were available throughout.

Adapted from Gandevia and McCloskey .] B, Detection of the direction of movements applied to the elbow under passive conditions (filled circles) and during a voluntary contraction (open circles) in two groups of subjects. Data from the passive condition used a slightly different definition of threshold from that during contraction. Adapted from Taylor and McCloskey
Figure 11. Figure 11.

A, Correlation between the reflex effects produced by digital nerve stimuli (upper panels) and the changes in perceived heaviness (lower panels). Stimuli at low intensity [twice sensory threshold (2T)] are innocuous and produce reflex inhibition of low‐threshold motoneurons (type S) and excitation of high‐threshold motoneurons (type F), whereas higher intensity stimuli (at 4T) are slightly painful and produce widespread inhibition of the motoneuron pool. Weights were lifted by abduction of the index finger (first dorsal interosseous muscle) with stimuli delivered to the digital nerves of the index finger. Nett reflex inhibition by cutaneous afferents increases perceived heaviness, although the absolute heaviness of the reference weight is unaltered. [Data from Aniss, Gandevia, and Milne .] B, Schematic representation of responses when subjects match the perceived effort (left panel) and perceived tension (right panel) produced by elbow flexion under isometric conditions. The reference force (solid line) was produced with the aid of visual feedback. A tonic vibration reflex was used to “assist” the contraction of the agonist elbow flexors as indicated by the horizontal bars. If the subject matched the perceived effort required to match the reference force, the matching force diminished, but if required, the subject could accurately match the perceived isometric force during the reflex assistance to movement when the effort required to maintain it had diminished.

Based on McCloskey, Ebeling, and Goodwin
Figure 12. Figure 12.

Attempted “focusing” by one subject on either abductor digiti minimi (muscle 1) or abductor digiti minimi (muscle 2). Sketch at lower right shows the simultaneous recording from the two muscles. The subject attempted this without recruitment of the lowest threshold motor units (recorded with needle electrodes) and thus there was no movement‐related feedback. At unpredictable times, a weak transcranial stimulus to the contralateral motor cortex tested the success of focusing. Nine trials from one continuous sequence are shown. Upper trace in each pair is from abductor digiti minimi (muscle 1) and lower trace from abductor pollicis brevis (muscle 2). Upward arrow and dotted lines indicate the timing of stimuli to the motor cortex (delivered only when both muscles were electromyographically silent). In the first column (trials a–d) the subject focused on muscle 1. On the first trial (a), the cortical stimulus failed to evoke activity in either muscle. On the next three trials, the subject successfully achieved activity in muscle 1 without discharging muscle 2. The instruction was then changed to focus on muscle 2. After three successful trials (e–g), the instruction was reversed.

Adapted from Gandevia and Rothwell
Figure 13. Figure 13.

Results from three lifting combinations in which flexor digitorum profundus lifted a reference weight of 200 g on the reference side. In experimental trials a weight was also lifted concurrently on the same side, and in control trials no concurrent weight was lifted. The perceived heaviness of the reference weight was always determined by matching it to a variable weight lifted by thumb flexion on the contralateral side. Data obtained when the fingers lifting the reference and concurrent weight were anesthetized (open circles), and for combination when sensation was intact (filled circles). Mean (± SEM) for a group of subjects. The finger that lifted the reference weight is indicated at the top of the panel, and the finger that lifted the concurrent weight at the bottom. Perceived heaviness of the reference weight increases when a neighboring finger lifts concurrently, even when the digits are anesthetized.

Adapted from Kilbrath and Gandevia
Figure 14. Figure 14.

Accuracy of matching weights in a group of subjects with four muscles [flexor pollicis longus (FPL), flexor digitorum longus acting on the index finger (FDP index), adductor pollicis (AP) and first dorsal interosseous (FDI)] at several fractions of maximal voluntary force (MVC). Reference weights lifted on one side were matched with variable weights lifted with the corresponding muscle on the contralateral side. Accuracy derived from the coefficient of variation of repeated lifts (mean ± SEM). A, Accuracy for the four different muscles. Flexor pollicis longus showed significantly higher accuracy than the other muscles. 6, Matching over a wide range of weights for FPL (open circles) and FDP index (filled circles). Even at very low forces (< 1 % MVC, open square) accuracy is maintained for FPL.

Adapted from Kilbreath and Gandevia
Figure 15. Figure 15.

Dissociation of the perceived command to move and the perceived time at which the muscle actually contracted. The subject makes intermittent contractions of a hand muscle, and around the time they occur a reference stimulus is delivered to the foot. Timing of the reference stimulus for perceived simultaneity can be deduced from repeated trials. Upper panel shows when the subject believes that the command to move and the stimulus occur simultaneously. Lower panel shows when the subject believes that the actual movement and the stimulus occur simultaneously. Traces in the two conditions aligned with the voluntary EMG to show that, for the command to move to occur at the same time as the reference stimulus, the stimulus precedes the EMG, but for the actual movement to seem first, the reference stimulus comes after the EMG. When the EMG coincided with the stimulus, the command to move was perceived to occur first, whereas the reference stimulus had to occur some 100 ms later (i.e., well into the contraction) for the actual movement to seem first.

Based on McCloskey et al.
Figure 16. Figure 16.

At left, The two eyes are shown while the subject looks straight ahead but with vision prevented by a cover over the right eye. The subject viewed targets moving slowly from the left or right (horizontal arrows) and indicated when they appeared directly in front (i.e., straight ahead) (open circle). At right, The right eye has been rotated 30 degrees to the right via a corneal lens, but it remains covered. Visual “straight ahead” is now judged to be ∼5 degrees to the right (i.e., in the direction of the deviated and covered eye). Note there was no reflex change in position of the uncovered left eye. Despite the deviation in visual localization, there was no sensation that eye position had changed.

Adapted from Gauthier, Nommay, and Vercher
Figure 17. Figure 17.

Blood pressure and heart rate records in a subject with all muscles completely paralyzed with a high‐dose infusion of atracurium during attempted contractions of the paralyzed dorsiflexors of the ankle. Supramaximal stimulation of the phrenic nerve confirmed that paralysis was complete. Attempted contractions at 100%, 50%, and 25% of maximum. The effect of a sham maneuver consisting of verbal encouragement but no attempted contraction is included (“0%”). Solid bars indicate the duration of each test period. Cardiovascular responses are graded with the level of motor command or effort. This effect must be due to motor commands and cannot be due to co‐contraction of remote muscles.

From Gandevia et al.
Figure 18. Figure 18.

Recording of the motor output to a completely paralyzed muscle. Microneurographic recordings were made from tibialis anterior motor axons when the whole common peroneal nerve was blocked distal to the recording site with local anesthetic. Muscle afferent feedback was thus acutely removed and attempted dorsiflexion of the ankle produced no movement. A, Raw and integrated neurogram directed to tibialis anterior during 2 rapid maximal efforts (left) and subsequently during a sequence of five steps of increasing effort (right). This sequence ended with a maximal effort. B, Pooled data for step sequences of effort with auditory feedback of the neurogram from five subjects (open symbols, solid line) and without (hatched line). Note that the initial step is larger in the absence of auditory feedback as is the decline in neurogram within each step. C, Performance when attempting a matching effort on the paralyzed and the normal side is not the same for rising and falling forces. Neurogram from the paralyzed side and force recorded simultaneously from the dorsiflexors on the contralateral side. For rising forces the neurogram is excessive, and for falling forces it is too low. Under control conditions subjects can produce closely correlated ramps of increasing then decreasing effort.

From Gandevia et al. , with permission
Figure 19. Figure 19.

A, Data from a model of acute arthritis in the cat knee. Joint afferents in the medial articular nerve, classified according to conduction velocity, studied under control conditions (filled symbols) and during acute inflammation (open symbols). The percentages of units with a background discharge in the midrange (circles), responsiveness to non‐noxious (squares) and noxious movements (triangles) are shown. [Data from Dorn, Schaible, and Schmidt .] B, At left. Mean values (± SEM) for estimates of position sense at the proximal interphalangeal joint of the index finger (PIP) in subjects with rheumatoid arthritis and a matched control group. Subjects aligned a silhouette to the perceived position of the passively displaced joint (0.3 degree/s). Errors were usually in the direction of the flexion deformity. [Data from Ferrell, Crighton, and Sturrock .] At right, Mean values (± SEM) for estimates of position sense at the knee in subjects with knee replacement and an age‐matched control group. The test relied on active reproduction of a passively imposed position.

Data from Barrack et al.
Figure 20. Figure 20.

Schematic representation of the destinations for both afferent and efferent kinesthetic signals.



Figure 1.

Schematic representation of one efference copy mechanism used by mormyrid fish. The electric organ discharges in response to the command from the electric organ discharge nucleus and this evokes a reafferent signal in the knollenorgan receptor. Environmentally mediated events evoke exafferent signals in this receptor. The efference copy acts as an exact inhibitory template to block reafferent signals so that the fish can more easily detect the environmental signals. Here, the corollary discharge provides a precise template of the expected reafference (see text).

Adapted from Bell


Figure 2.

Modulation of muscle spindle discharge by small length changes diminishes markedly when they are superimposed on slow movements. Data from a population of primary spindle afferents innervating the cat soleus muscle to illustrate the effects of an underlying slow movement on the sensitivity to sinusoidal stretch delivered at about 1 Hz. Panels at left show the control sinusoidal stretch (upper trace) and the sinusoidal stretch delivered during a slow “triangular” movement (lower trace). Panels at right show the responses for a 50 μm (above) and 1,000 μm sinusoid (below). Responses to combined sinusoidal and triangular stretch shown as the median (thick line) with interquartile ranges. Open circle indicates the control responses without slow movement. Sensitivity scale is enlarged in the lower panel, with the cross in the upper panel indicating the corresponding response to 1,000 μm sinusoid during the fastest movement. These results mean that primary spindle afferents will encode large changes in length faithfully but will only respond dynamically to very small perturbations when the movement is very slow or isometric.

Adapted from Baumann and Hulliger


Figure 3.

A, Comparison between responses of a primary muscle spindle afferent and Golgi tendon organ in the cat soleus muscle to longitudinal vibration under control conditions and during a contraction produced by intense ventral root stimulation. The primary muscle spindle ending follows 1:1 the vibration at 400 Hz (10 m) under control conditions. Its discharge increases during contraction (due to fusimotor activation), but, during combined contraction and vibration, the response is less than under control conditions. The tendon organ requires larger amplitude vibration to respond at rest (200 Hz, 150 m), increases its discharge during muscle contraction, but, during combined contraction and vibration, the response is 1:1 and greater than under the control conditions. (Adapted from Brown, Engberg, and Matthews .] B, Behavior of a Golgi tendon organ afferent to vibration applied transversely to the tibialis anterior tendon at 40 Hz when the muscle is relaxed (upper panels) and during a weak voluntary contraction (lower panels). The unit responds at a subharmonic of the vibration frequency during relaxation but responds 1:1 with vibration during the contraction.

From Roll, Vedel, and Ribot .] While it is possible that the response of the Golgi tendon organ afferents shown in these two panels represents the extreme of their behavior, nonetheless, some will behave this way under natural conditions


Figure 4.

Responses of ten tendon organ afferents innervating peroneus tertius muscle in the cat to motor unit forces produced by stimulation of one or two motor units. A, Average tendon organ responses to the forces from motor unit A (left panel), motor unit B (middle panel), and both motor units (right panel). Stimuli given at 10, 20, and 40 Hz. Motor unit A activated six tendon organs and motor unit B activated four tendon organs (shared with motor unit A). Average tendon organ response calculated from the responses of the activated tendon organs. When both motor units contract to 40 Hz stimulation, force at the tendon adds as expected from the algebraic sum of the force to each motor unit, but the average discharge frequency does not exceed that when unit 2 contracts alone. Note that in the right panel the average tendon organ response to stimulation of both motor units at 20 Hz is less after the tetanus at 40 Hz.

Adapted from Jami .] B, Predicted ensemble response for the data in part A of the figure when the total number of tendon organ discharges is calculated (from their average discharge and the number activated). This has been estimated for the tetani produced by 40 Hz stimuli and the two sets of 20 Hz stimuli. Total tendon organ input increases very well with tendon force


Figure 5.

Behavior of a joint afferent from the proximal interphalangeal joint of the index finger recorded from the median nerve. Responses during passive rotation in the flexion‐extension axis. Inset shows a tonic discharge when the joint was in the rest position. Upper trace, Instantaneous frequency. Lower trace, Goniometer record. Note the sustained high‐frequency discharge when the joint was moved into extreme extension, with no change in background discharge when it moved into flexion but a sustained discharge when forced into extreme flexion. Many receptors of this type also responded to movements in the abduction‐adduction or extorsion‐intorsion axis.

Adapted from Burke, Gandevia, and Macefield


Figure 6.

A, Responses of a typical SA II afferent innervating the skin on the dorsum of the hand during voluntary flexion and extension of the metacarpophalangeal joint of the index finger. B, The receptive field and response to focal indentation of the skin. Despite its “remote” location, the afferent responds to the voluntary movements.

Adapted from Edin and Abbs .] C, Summary of the responsiveness of a sample of SA II cutaneous afferents innervating the dorsum of the hand and muscle spindle afferents from extensors of the index finger to movement of the metacarpophalangeal joint of the index finger with the muscles relaxed. The three vertical axes refer to different methods of measuring the static and dynamic sensitivity of the afferents to applied movements. From Grill and Hallert


Figure 7.

A, Movement illusions recorded when vibrators are applied to the distal tendons of the left biceps brachii and triceps brachii. Left arm is fixed and the right (tracking arm) is mobile and connected to a goniometer. The subject matches the perceived movement during vibration of the biceps tendon at different frequencies. The speed of the illusory extension movement increases with vibration frequency but diminishes at the highest frequency, presumably because the primary spindle afferents no longer follow 1:1 the vibrator frequency.

Adapted from Roll and Vedel .] B, Superimposed data from one subject for combinations of vibration applied simultaneously to the biceps and triceps muscles. Perceived movement of the vibrated arm depends on the difference in frequencies of vibration, with an illusory movement of extension when the vibration frequency is greater for the flexors than extensors. [Adapted from Gilhodes, Roll, and Tardy‐Gervet .] C, During trains of stimuli delivered to the ulnar nerve at the wrist (below motor threshold and without inducing cutaneous paresthesias), the subject experienced illusory flexion of the interphalangeal joints and extension of the metacarpophalangeal (MCP) joint. The complex illusory motion at three joints is consistent with perceived elongation of the interosseous and lumbrical muscles acting on the ring finger. The component at the MCP joint was measured with matching movements on the contralateral side. Relationship between stimulus frequency and perceived velocity for one subject. By comparison with A, the illusory movement (mean ± SEM) increases progressively even at stimulus frequencies above 100/s. This suggests that mechanical entrainment of spindle afferent discharge is impaired at higher vibration frequencies. Reproduced from Gandevia and Gandevia and Burke


Figure 8.

Position‐sense thresholds for detection of joint displacements at the metacarpophalangeal (MCP), proximal interphalangeal (PIP), and distal interphalangeal (DIP) joints of the middle finger in five subjects. Movements were delivered with the joint in the midrange at 2 degrees min (i.e., below the velocity at which movement sensations occur). Each point depicts data from one subject with filled circles for control performance under passive conditions and open circles for estimates when voluntary contraction of the flexors and extensors occurred after the final position had been reached. In one condition, the hand was postured so that the distal joint of the middle finger could not be moved by voluntary contractions and thus the joint was effectively disengaged from its attachments.

Adapted from Taylor and McCloskey


Figure 9.

A, Detection of 5‐degree movements at different angular velocities from a midposition of the distal interphalangeal joint of the middle finger. Subjects had to nominate correctly the direction of the movement. Mean data from references 55 and 91 have been pooled. Data with the hand postured so as to disengage the flexor and extensor muscles are shown as open circles . Filled circles represent performance when the distal interphalangeal joint was injected with local anesthetic. Performance is best when the muscle, joint, and cutaneous afferents are all intact (hatched horizontal bar): it deteriorates when muscles cannot contribute to movement detection and deteriorates further when the joint space is injected with local anesthetic. (From Gandevia and Burke .] B, Distribution of modular errors for the perceived position of the proximal interphalangeal joint of the index finger under control conditions (upper panel) and when the digital nerves of the finger had been blocked with local anesthetic (lower panel).

Adapted from Ferrell and Smith .] A schematic view of the perceived position of the proximal joint of the finger during digital anesthesia shown by the dashed lines. The range of perceived positions of the joint was compressed when joint and cutaneous afferents were anesthetized. C, Schematic representation of the distortion of position sense induced by a digital nerve block


Figure 10.

A, Detection of the direction of movements applied to the distal interphalangeal joint of the middle finger when the digit was anesthetized at its base (open circles) and when the subject exerted a weak flexor contraction with the anesthetized finger (filled circles). The hand was postured so that only contraction of the long flexor moved the joint. Proprioceptive acuity was restored to within the normal range when muscle contraction occurred in the absence of local joint and cutaneous inputs (compare Fig. A). Remote cutaneous signals were available throughout.

Adapted from Gandevia and McCloskey .] B, Detection of the direction of movements applied to the elbow under passive conditions (filled circles) and during a voluntary contraction (open circles) in two groups of subjects. Data from the passive condition used a slightly different definition of threshold from that during contraction. Adapted from Taylor and McCloskey


Figure 11.

A, Correlation between the reflex effects produced by digital nerve stimuli (upper panels) and the changes in perceived heaviness (lower panels). Stimuli at low intensity [twice sensory threshold (2T)] are innocuous and produce reflex inhibition of low‐threshold motoneurons (type S) and excitation of high‐threshold motoneurons (type F), whereas higher intensity stimuli (at 4T) are slightly painful and produce widespread inhibition of the motoneuron pool. Weights were lifted by abduction of the index finger (first dorsal interosseous muscle) with stimuli delivered to the digital nerves of the index finger. Nett reflex inhibition by cutaneous afferents increases perceived heaviness, although the absolute heaviness of the reference weight is unaltered. [Data from Aniss, Gandevia, and Milne .] B, Schematic representation of responses when subjects match the perceived effort (left panel) and perceived tension (right panel) produced by elbow flexion under isometric conditions. The reference force (solid line) was produced with the aid of visual feedback. A tonic vibration reflex was used to “assist” the contraction of the agonist elbow flexors as indicated by the horizontal bars. If the subject matched the perceived effort required to match the reference force, the matching force diminished, but if required, the subject could accurately match the perceived isometric force during the reflex assistance to movement when the effort required to maintain it had diminished.

Based on McCloskey, Ebeling, and Goodwin


Figure 12.

Attempted “focusing” by one subject on either abductor digiti minimi (muscle 1) or abductor digiti minimi (muscle 2). Sketch at lower right shows the simultaneous recording from the two muscles. The subject attempted this without recruitment of the lowest threshold motor units (recorded with needle electrodes) and thus there was no movement‐related feedback. At unpredictable times, a weak transcranial stimulus to the contralateral motor cortex tested the success of focusing. Nine trials from one continuous sequence are shown. Upper trace in each pair is from abductor digiti minimi (muscle 1) and lower trace from abductor pollicis brevis (muscle 2). Upward arrow and dotted lines indicate the timing of stimuli to the motor cortex (delivered only when both muscles were electromyographically silent). In the first column (trials a–d) the subject focused on muscle 1. On the first trial (a), the cortical stimulus failed to evoke activity in either muscle. On the next three trials, the subject successfully achieved activity in muscle 1 without discharging muscle 2. The instruction was then changed to focus on muscle 2. After three successful trials (e–g), the instruction was reversed.

Adapted from Gandevia and Rothwell


Figure 13.

Results from three lifting combinations in which flexor digitorum profundus lifted a reference weight of 200 g on the reference side. In experimental trials a weight was also lifted concurrently on the same side, and in control trials no concurrent weight was lifted. The perceived heaviness of the reference weight was always determined by matching it to a variable weight lifted by thumb flexion on the contralateral side. Data obtained when the fingers lifting the reference and concurrent weight were anesthetized (open circles), and for combination when sensation was intact (filled circles). Mean (± SEM) for a group of subjects. The finger that lifted the reference weight is indicated at the top of the panel, and the finger that lifted the concurrent weight at the bottom. Perceived heaviness of the reference weight increases when a neighboring finger lifts concurrently, even when the digits are anesthetized.

Adapted from Kilbrath and Gandevia


Figure 14.

Accuracy of matching weights in a group of subjects with four muscles [flexor pollicis longus (FPL), flexor digitorum longus acting on the index finger (FDP index), adductor pollicis (AP) and first dorsal interosseous (FDI)] at several fractions of maximal voluntary force (MVC). Reference weights lifted on one side were matched with variable weights lifted with the corresponding muscle on the contralateral side. Accuracy derived from the coefficient of variation of repeated lifts (mean ± SEM). A, Accuracy for the four different muscles. Flexor pollicis longus showed significantly higher accuracy than the other muscles. 6, Matching over a wide range of weights for FPL (open circles) and FDP index (filled circles). Even at very low forces (< 1 % MVC, open square) accuracy is maintained for FPL.

Adapted from Kilbreath and Gandevia


Figure 15.

Dissociation of the perceived command to move and the perceived time at which the muscle actually contracted. The subject makes intermittent contractions of a hand muscle, and around the time they occur a reference stimulus is delivered to the foot. Timing of the reference stimulus for perceived simultaneity can be deduced from repeated trials. Upper panel shows when the subject believes that the command to move and the stimulus occur simultaneously. Lower panel shows when the subject believes that the actual movement and the stimulus occur simultaneously. Traces in the two conditions aligned with the voluntary EMG to show that, for the command to move to occur at the same time as the reference stimulus, the stimulus precedes the EMG, but for the actual movement to seem first, the reference stimulus comes after the EMG. When the EMG coincided with the stimulus, the command to move was perceived to occur first, whereas the reference stimulus had to occur some 100 ms later (i.e., well into the contraction) for the actual movement to seem first.

Based on McCloskey et al.


Figure 16.

At left, The two eyes are shown while the subject looks straight ahead but with vision prevented by a cover over the right eye. The subject viewed targets moving slowly from the left or right (horizontal arrows) and indicated when they appeared directly in front (i.e., straight ahead) (open circle). At right, The right eye has been rotated 30 degrees to the right via a corneal lens, but it remains covered. Visual “straight ahead” is now judged to be ∼5 degrees to the right (i.e., in the direction of the deviated and covered eye). Note there was no reflex change in position of the uncovered left eye. Despite the deviation in visual localization, there was no sensation that eye position had changed.

Adapted from Gauthier, Nommay, and Vercher


Figure 17.

Blood pressure and heart rate records in a subject with all muscles completely paralyzed with a high‐dose infusion of atracurium during attempted contractions of the paralyzed dorsiflexors of the ankle. Supramaximal stimulation of the phrenic nerve confirmed that paralysis was complete. Attempted contractions at 100%, 50%, and 25% of maximum. The effect of a sham maneuver consisting of verbal encouragement but no attempted contraction is included (“0%”). Solid bars indicate the duration of each test period. Cardiovascular responses are graded with the level of motor command or effort. This effect must be due to motor commands and cannot be due to co‐contraction of remote muscles.

From Gandevia et al.


Figure 18.

Recording of the motor output to a completely paralyzed muscle. Microneurographic recordings were made from tibialis anterior motor axons when the whole common peroneal nerve was blocked distal to the recording site with local anesthetic. Muscle afferent feedback was thus acutely removed and attempted dorsiflexion of the ankle produced no movement. A, Raw and integrated neurogram directed to tibialis anterior during 2 rapid maximal efforts (left) and subsequently during a sequence of five steps of increasing effort (right). This sequence ended with a maximal effort. B, Pooled data for step sequences of effort with auditory feedback of the neurogram from five subjects (open symbols, solid line) and without (hatched line). Note that the initial step is larger in the absence of auditory feedback as is the decline in neurogram within each step. C, Performance when attempting a matching effort on the paralyzed and the normal side is not the same for rising and falling forces. Neurogram from the paralyzed side and force recorded simultaneously from the dorsiflexors on the contralateral side. For rising forces the neurogram is excessive, and for falling forces it is too low. Under control conditions subjects can produce closely correlated ramps of increasing then decreasing effort.

From Gandevia et al. , with permission


Figure 19.

A, Data from a model of acute arthritis in the cat knee. Joint afferents in the medial articular nerve, classified according to conduction velocity, studied under control conditions (filled symbols) and during acute inflammation (open symbols). The percentages of units with a background discharge in the midrange (circles), responsiveness to non‐noxious (squares) and noxious movements (triangles) are shown. [Data from Dorn, Schaible, and Schmidt .] B, At left. Mean values (± SEM) for estimates of position sense at the proximal interphalangeal joint of the index finger (PIP) in subjects with rheumatoid arthritis and a matched control group. Subjects aligned a silhouette to the perceived position of the passively displaced joint (0.3 degree/s). Errors were usually in the direction of the flexion deformity. [Data from Ferrell, Crighton, and Sturrock .] At right, Mean values (± SEM) for estimates of position sense at the knee in subjects with knee replacement and an age‐matched control group. The test relied on active reproduction of a passively imposed position.

Data from Barrack et al.


Figure 20.

Schematic representation of the destinations for both afferent and efferent kinesthetic signals.

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Simon C. Gandevia. Kinesthesia: Roles for Afferent Signals and Motor Commands. Compr Physiol 2011, Supplement 29: Handbook of Physiology, Exercise: Regulation and Integration of Multiple Systems: 128-172. First published in print 1996. doi: 10.1002/cphy.cp120104