Lee D. Walsh

Proprioceptive signals contribute to the sense of body ownership.

Non‐technical summary  The sense of body ownership tells us that our body belongs to us, and other bodies do not. That our body belongs to us is fundamental to self‐awareness. It is known that synchronous touch and vision can be used to induce an illusion of ownership over an artificial rubber hand. Like the skin receptors used for touch, sensory receptors in the muscles only provide information about events occurring to the body. Whether muscle receptors contribute to our sense of body ownership is not known. This study developed a technique to induce an illusion of ownership over a plastic finger using movement, which excites muscle receptors. This sense of ownership still occurred when the contribution of skin and joint receptors was removed using local anaesthetic. The results clearly show that muscle receptors can contribute to the sense of body ownership.

Effect of a peripheral nerve block on torque produced by repetitive electrical stimulation

Neuromuscular electrical stimulation (NMES) generates contractions by activation of motor axons (peripheral mechanism), but the afferent volley also contributes by recruiting spinal motoneurons synaptically (central mechanism), which recruits motoneurons according to Hennemans size principle. Thus, we hypothesized that contractions that develop due to a combination of peripheral and central mechanisms will fatigue less rapidly than when electrically evoked contractions are generated by the activation of motor axons alone. Plantar-flexion torque evoked by NMES over the triceps surae was compared in five able-bodied subjects before (Intact) and during (Blocked) a complete anesthetic block of the tibial and common peroneal nerves. In the Blocked condition, plantar-flexion torque could only develop from the direct activation of motor axons beneath the stimulating electrodes. NMES was delivered using three protocols: protocol A, constant 100 Hz for 30 s; protocol B, four 2-s bursts of 100 Hz alternating with 20-Hz stimulation; and protocol C, alternating 100 Hz bursts (1 s on, 1 s off) for 30 s. The percent change in evoked plantar flexion torque from the beginning to the end of the stimulation differed (P < 0.05) between Intact and Blocked conditions for all protocols (Intact: protocol A = +125%, B = +230%, C = +78%; Blocked: protocol A = -79%, B = -15%, C = -35%). These results corroborate previous evidence that NMES can evoke contractions via the recruitment of spinal motoneurons in addition to the direct recruitment of motor axons. We now show that NMES delivered for periods of up to 30 s generates plantar-flexion torque which decreases when only motor axons are recruited and increases when the central nervous system can contribute.

High-frequency submaximal stimulation over muscle evokes centrally generated forces in human upper limb skeletal muscles

Control of posture and movement requires control of the output from motoneurons. Motoneurons of human lower limb muscles exhibit sustained, submaximal activity to high-frequency electrical trains, which has been hypothesized to be partly triggered by monosynaptic Ia afferents. The possibility to trigger such behavior in upper limb motoneurons and the potential unique role of Ia afferents to trigger such behavior remain unclear. Subjects (n = 9) received high-frequency trains of electrical stimuli over biceps brachii and flexor pollicis longus (FPL). We chose to study the FPL muscle because it has weak monosynaptic Ia afferent connectivity and it is involved in fine motor control of the thumb. Two types of stimulus trains (100-Hz bursts and triangular ramps) were tested at five intensities below painful levels. All subjects exhibited enhanced torque in biceps and FPL muscles after both types of high-frequency train. Torques also persisted after stimulation, particularly for the highest stimulus intensity. To separate the evoked torques that resulted from a peripheral mechanism (e.g., muscle potentiation) and that which resulted from a central origin, we studied FPL responses to high-frequency trains after complete combined nerve blocks of the median and radial nerves (n = 2). During the blocks, high-frequency trains over the FPL did not yield torque enhancements or persisting torques. These results suggest that enhanced contractions of central origin can be elicited in motoneurons innervating the upper limb, despite weak monosynaptic Ia connections for FPL. Their presence in a recently evolved human muscle (FPL) indicates that these enhanced contractions may have a broad role in controlling tonic postural outputs of hand muscles and that they may be available even for fine motor activities involving the thumb.

Illusory movements of a phantom hand grade with the duration and magnitude of motor commands.

The senses of limb movement and position are critical for accurate control of movement. Recent studies show that central signals of motor command contribute to the sense of limb position but it is not clear whether such signals influence the distinctly different sense of limb movement. Nine subjects participated in two experiments in which we inflated a cuff around their upper arm to produce an ischaemic block, paralysing and anaesthetising the forearm, wrist and hand. This produces an experimental phantom wrist and hand. With their arm hidden from view subjects were asked to make voluntary efforts with their blocked wrist. In the first experiment, efforts were 20 and 40% of maximum and were 2 and 4 s in duration. The second experiment used 1 and 5 s efforts of 5 and 50% of maximum. Subjects signalled perceived movements of their phantom wrist using a pointer. All subjects reported clear perceptions of movement of their phantom hand for all levels and durations of effort. On average, subjects perceived their phantom wrist to move between 16.4 ± 3.3 deg (mean ± 95% confidence interval (CI)) and 30.2 ± 5.4 deg in the first experiment and between 10.3 ± 3.5 and 38.6 ± 6.7 deg in the second. The velocity of the movements and total displacement of the phantom graded with the level of effort, and the total displacement also graded with duration. Hence, we have shown that motor command signals have a novel proprioceptive role in the perception of movement of human joints.

The combined effect of muscle contraction history and motor commands on human position sense.

Along with afferent information, centrally generated motor command signals may play a role in joint position sense. Isometric muscle contractions can produce a perception of joint displacement in the same direction as the joint would move if unrestrained. Contradictory findings of perceived joint displacement in the opposite direction have been reported. As this only occurs if muscle spindle discharge in the contracting muscle is initially low, it may reflect increased muscle spindle firing from fusimotor activation, rather than central motor command signals. Methodological differences including the muscle contraction task and use of muscle conditioning could underlie the opposing findings. Hence, we tested perceived joint position during two contraction tasks (‘hold force’ and ‘hold position’) at the same joint (wrist) and controlled muscle spindle discharge with thixotropic muscle conditioning. We expected that prior conditioning of the contracting muscle would eliminate any effect of increased fusimotor activation, but not of central motor commands. Muscle conditioning altered perceived wrist position as expected. Further, during muscle contractions, subjects reported wrist positions displaced ~12° in the direction of contraction, despite no change in wrist position. This was similar for ‘hold force’ and ‘hold position’ tasks and occurred despite prior conditioning of the agonist muscle. However, conditioning of the antagonist muscle did reduce the effect of voluntary contraction on position sense. The errors in position sense cannot be explained by fusimotor activation. We propose that central signals combine with afferent signals to determine limb position and that multiple sources of information are weighted according to their reliability.

Dynamic changes in the perceived posture of the hand during ischaemic anaesthesia of the arm

Non‐technical summary  Even when the hand is stationary we know its position. This information is needed by the brain to plan movements. If the sensory input from a limb is removed through an accident, or an experiment with local anaesthesia, then a ‘phantom’ limb commonly develops. We used ischaemic anaesthesia of one arm to study the mechanisms which define the phantom hand. Surprisingly, if the wrist and fingers are held straight during anaesthesia, the perceived phantom hand becomes bent at the wrist and fingers, but if they are bent during anaesthesia, the final phantom is extended at the wrist and fingers. There is no ‘default’ posture for the phantom hand. Further, the hand appears to increase gradually in size as anaesthesia develops. The start of these perceptual changes occurs when input from large‐diameter sensory nerve fibres is declining. These results provide new information about how the brain generates phantom limbs.

Overestimation of force during matching of externally generated forces

If a weight is applied to a finger and the subject asked to produce the same force, the subject generates a force larger than the weight. That is, subjects overestimate the force applied by an external target when matching it. Details of this force overestimation are not well understood. We show that subjects overestimate small target weights, but not larger ones. Furthermore we show for the first time that the force overestimation consists of two components. The first component is a constant. The second component depends on the precise magnitude of the weight and is only present when subjects hold the target weight against gravity. We suggest that the two components are generated in different phases of the force‐matching task, are due to different processes, and must have an influence on all proprioceptive judgements of force.

The contribution of motor commands to position sense differs between elbow and wrist.

•  Knowing the position of our limbs is critical for accurate movement. Central motor command signals generated by the brain contribute to position sense at the human wrist, but this could not be demonstrated at the elbow. •  We tested whether this represents a fundamental difference between the two joints or whether it reflects the two different methods used to measure position sense. •  For both measurement methods, contraction of wrist muscles led to illusions that the wrist is displaced. No such illusions were detected at the elbow during muscle contraction. •  Thus, the contribution of centrally generated command signals to position sense differs between joints. Any contribution at the elbow joint is small and new methods will be needed to reveal it.

New display of the timing and firing frequency of single motor units

The neural control of important rhythmical processes such as breathing and locomotion is complex. It is often necessary to depict the activity of motor (or other) units throughout the cycles. We describe and illustrate a novel method that displays visually seven key variables in a single figure related to the timing and frequencies of the discharge of single motor units. This time-and-frequency plot (TAFPLOT) displays the recruitment time, time of peak discharge frequency and derecruitment time, as well as the onset, peak, and final firing frequencies of each motor unit in a population. The frequency of any tonic firing is also displayed. Using the TAFPLOT it is easy to identify the presence or absence of coordinated activity within and between different motoneuron pools. The method is used to illustrate novel differences in the discharge behavior between populations of single motor units innervating the human diaphragm and genioglossus muscles. This new display provides a simple, qualitative and quantitative tool to study the neural control of rhythmical or repetitive motor tasks.

Is this my finger? Proprioceptive illusions of body ownership and representation

•  The brain keeps a representation of which things are part of our body. This sense of ownership is easily manipulated using brushing of the skin or movement of a limb to create an illusion of ownership over an inanimate object, such as a rubber hand. •  We induced a sense of ownership of an artificial finger using movement of the index finger without vision of the hands. As cutaneous receptors had been anaesthetised, this illusion depended on proprioceptive signals from muscle receptors. •  In addition, we found a new grasp illusion in which perceived distance between the index fingers decreases when subjects hold an artificial finger. •  These results increase understanding of how the brain generates our body representation and may help in understanding diseases in which the sense of ownership is disrupted.