Jonathan Cole

Dissociated secondary hyperalgesia in a subject with a large-fibre sensory neuropathy

&NA; In the skin surrounding a site of injury, hyperalgesia develops to mechanical stimuli. Two types of secondary hyperalgesia (to light touch and punctate stimuli) have recently been differentiated, based on different durations and sizes of the area involved. We studied secondary hyperalgesia in a subject who had a loss of myelinated afferent nerve fibres below the neck that spared the A&dgr; group. Stroking with a cotton swab was not perceived anywhere on affected skin either before or after injection of 60 &mgr;g of capsaicin. Thus, there was no hyperalgesia to light touch. Capsaicin injection into the volar forearm evoked normal pain and flare. A von Frey probe exerting a force of 40 mN was perceived as sharp. The sensation of sharpness was more pronounced up to 2 cm outside the flare zone for at least 16 min following the injection (tested with a 200 mN von Frey probe). Thus, hyperalgesia to punctate stimuli developed as in healthy subjects. These data support the model that hyperalgesia to light touch (allodynia) is due to sensitisation of central pain‐signaling neurones to low‐threshold mechanoreceptor input (A&bgr; fibres). In contrast, punctate hyperalgesia is likely to be due to sensitisation to nociceptor input (A&dgr; or C fibres).

Control of single-joint movements in deafferented patients: evidence for amplitude coding rather than position control

Two deafferented patients and several control subjects participated in a series of experiments to investigate how accurate single-joint movements are programed, spatially calibrated, and updated in the absence of proprioceptive information. The deafferented patients suffered from a permanent and severe loss of large sensory myelinated fibers below the neck. Subjects performed, with and without vision, sequences of forearm supinations and pronations with two temporal delays between each movement (0 s and 8 s). Overall, the lack of proprioception did not yield any significant decrease in movement accuracy when vision was available. Without vision, the absence of proprioceptive afferents yielded (1) significantly larger spatial errors, (2) amplitude errors similar to those of control subjects, and (3) a significant drift when an 8-s delay was introduced between two successive movements. Subjects also performed, without vision, a 20∘ supination followed by a 20∘ pronation that brought back the wrist to the starting position. On some trials, the supination was blocked unexpectedly by way of a magnetic brake. When the supination was blocked, subjects were already on the second target and no pronation was required when the brake was released. The defferented patients, unaware of the procedure, always produced a 20∘ pronation. These data confirm that deafferented patients were not coding a final position. It rather suggests that they coded an amplitude and translated the spatial distance between the two targets in a corresponding force pulse. Overall, the results highlight the powerful and key role of proprioceptive afferents for calibrating the spatial motor frame of reference.

Evidence for stronger visuo-motor than visuo-proprioceptive conflict during mirror drawing performed by a deafferented subject and control subjects

It has been proposed that mirror drawing is difficult because of the conflict between visual and proprioceptive signals from the arm. However, even without proprioception, there should be difficulties in planning movements to visual targets observed in a mirror, as the mirror-reversed spatial information must be translated into appropriate hand actions. Mirror drawing tasks suggest these planning conflicts are likely to be most obvious at corners, when encountering sharp changes in direction. We have therefore tested the speed of mirror drawing in a chronically deafferented man and in a control group of normal subjects, and hypothesized that increases in template complexity (number of corners) would result in reduced drawing speeds in all subjects. Indeed, all subjects, including the deafferented man, showed movement durations that increased linearly as the complexity of the drawings increased. However, the deafferented man was significantly faster than the control subjects at tracing curved templates. We suggest that the major difficulty in mirror tracking is in the visuo-motor planning of actions based on mirror-reversed visual information, and is not a conflict between visual and proprioceptive signals about arm motion.

The relative contribution of retinal and extraretinal signals in determining the accuracy of reaching movements in normal subjects and a deafferented patient

This experiment investigated the relative extent to which different signals from the visuo-oculomotor system are used to improve accuracy of arm movements. Different visuo-oculomotor conditions were used to produce various retinal and extraretinal signals leading to a similar target amplitude: (a) fixating a central target while pointing to a peripheral visual target, (b) tracking a target through smooth pursuit movement and then pointing to the target when its excursion ceased, and (c) pointing to a target reached previously by a saccadic eye movement. The experiment was performed with a deafferented subject and control subjects. For the deafferented patient, the absence of proprioception prevented any comparison between internal representations of target and limb (through proprioception) positions during the arm movement. The deafferented patients endpoint therefore provided a good estimate of the accuracy of the target coordinates used by the arm motor system. The deafferented subject showed relatively good accuracy by producing a saccade prior to the pointing, but large overshooting in the fixation condition and undershooting in the pursuit condition. The results suggest that the deafferented subject does use oculomotor signals to program arm movement and that signals associated with fast movements of the eyes are better for pointing accuracy than slow ramp movements. The inaccuracy of the deafferented subject when no eye movement is allowed (the condition in which the controls were the most accurate) suggests that, in this condition, a proprioceptive map is involved in which both the target and the arm are represented.

Evidence of a limited visuo-motor memory used in programming wrist movements

Human subjects can pre-program movements on the basis of visual cues. Experience in a particular task leads to the storage of appropriate control parameters which are used in programming subsequent movements, via a short-term motor memory. The form, duration and usage of this memory are, however, uncertain. Repetitive wrist flexion and extension movements were measured in four subjects. Three were neurologically normal men; the fourth subject had a peripheral large-fibre sensory neuropathy, depriving him of proprioceptive information about wrist movement. Subjects made alternating 45° wrist movements between two visual targets; visual feedback of wrist position was provided for the first part of each trial. After 10 s of tracking, the subjects paused for an interval of 0–24 s before resuming tracking without visual feedback of wrist position. The positional accuracy of subsequent movements was analysed with respect to pause interval. Movement accuracy was reduced by the removal of visual feedback in all four subjects: movements after the pause interval were less accurate than those before the pause. Errors also accumulated within each sequence of movements made without visual feedback. Analysis of the first movement in each trial after the pause indicated a clear relationship between movement accuracy and pause interval. In all four subjects, movement accuracy decayed with longer pause intervals. In the deafferented subject, manipulation of the visual inputs (requiring visual fixation, rather than normal pursuit of the target; or direct viewing of the hand instead of viewing a cursor on a computer screen) affected the relationship between pause interval and subsequent movement accuracy. We propose that the memory used when producing these movements is a short-lasting visuo-motor signal, lasting a few seconds, which is derived from visual knowledge of previous movements, rather than a memory of a particular motor output. This visuo-motor signal is used to scale the amplitude of subsequent wrist movements. The brevity of the visuo-motor memory and the resultant inaccuracy of this deafferented subject and of our neurologically normal subjects implies that human feedforward control of the amplitude and position of wrist movements is severely limited.

Adaptation in visuomanual tracking depends on intact proprioception.

The role of arm proprioception in motor learning was investigated in experiments in which, by moving the arm, subjects followed the motion of a target displayed on a monitor screen. Adaptive capabilities were tested in visuomanual tracking tasks following alterations in the relationship between the observers actual arm movement and visual feedback of the arm movement given by a cursor motion on the screen. Tracking performance and adaptive changes, measured in terms of spatiotemporal error, tracking trajectory curvature, and spatial gain, were compared in 7 control subjects (CSs) and in 1 deafferented subject (DS). CSs adapted appropriately to altered visuomanual relationships; those changes were present in trials immediately after restoration of normal scaling. In contrast, although the DS modified his tracking strategy from trial to trial according to the altered conditions, he did not show plastic changes in internal visuomanual scaling. Like the results of prismatic adaptation experiments, the present results suggest that arm proprioception contributes to the plastic changes that follow alterations in the scaling of visuomanual gain.

Does the oculo-manual co-ordination control system use an internal model of the arm dynamics?

The hypothesis that during self-moved target tracking, the eye-arm co-ordination control system uses an internal model of the arm dynamics was tested. The contribution of arm proprioception to this model was also assessed. Subjects (nine healthy adults and one deafferented subject) were requested to make forearm movements and visually track an arm-driven target. Unexpected changes in mechanical properties of the manipulandum were used to modify the dynamical conditions of arm movement. The smooth pursuit gain (SPG) was computed before and during the perturbation. Results showed a decrease of SPG during perturbation in control subjects only. We propose that an internal model of the arm dynamics may be used to co-ordinate eye and arm movements, and arm proprioception may contribute to this internal model.

Role of arm proprioception in calibrating the arm-eye temporal coordination

When subjects track with the eyes an arm-attached target, eye latency is shorter than when tracking an external target. This improved synchrony could result from either a common command addressed to the two systems or from an influence of the arm command on eye motion initiation. According to the first hypothesis, the eyes should start moving long before the arm, because of the difference in dynamics. We recorded arm and eye motion together with biceps muscle activity in controls and a deafferented subject. Data support the second hypothesis. Moreover, the deafferented subject showed a lesser correlation between arm and eye motions than controls, suggesting a role for arm proprioception in the calibration of the temporal relationship between arm and eye movements.