Deafferented Patients Research Articles

Somatosensory Loss Influences the Adoption of Self-Centered Versus Decentered Perspectives.

The body and the self are commonly experienced as forming a unity. Experiencing the external world as distinct from the self and the body strongly relies on adopting a single self-centered perspective which results in integrating multisensory sensations into one egocentric body-centered reference frame. Body posture and somatosensory representations have been reported to influence perception and specifically the reference frame relative to which multisensory sensations are coded. In the study reported here, we investigated the role of somatosensory and visual information in adopting self-centered and decentered spatial perspectives. Two deafferented patients who have neither tactile nor proprioceptive perception below the head and a group of age-matched control participants performed a graphesthesia task, consisting of the recognition of ambiguous letters (b, d, p, and q) drawn tactilely on head surfaces. To answer which letter was drawn, the participants can adopt either a self-centered perspective or a decentered one (i.e., centered on a body part or on an external location). The participants’ responses can be used, in turn, to infer the way the left-right and top-bottom letters’ axes are assigned with respect to the left-right and top-bottom axes of their body. In order to evaluate the influence of body posture, the ambiguous letters were drawn on the participants’ forehead, left, and right surfaces of the head, with the head aligned or rotated in yaw relative to the trunk. In order to evaluate the role of external information, the participants completed the task with their eyes open in one session and closed in another one. The results obtained in control participants revealed that their preferred perspective varied with body posture but not with vision. Different results were obtained with the deafferented patients who overall do not show any significant effect of their body posture on their preferred perspective. This result suggests that the orientation of their self is not influenced by their physical body. There was an effect of vision for only one of the two patients. The deafferented patients rely on strategies that are more prone to interindividual differences, which highlights the crucial role of somatosensory information in adopting self-centered spatial perspectives.

Inferences on the role of proprioception for perception and action by studying deafferented patients

Inferences on the role of proprioception for perception and action by studying deafferented patients

Neuromuscular reorganization after arm amputation revealed by stump EMG evoked by different phantom movements

Proprioception, the sense of position and movement of body segments, may not be known as much as other senses such as vision or audition. However, since the pioneer work of Sherrington, the critical role of proprioception in motor control has been increasingly highlighted. In particular, studies of human subjects massively deprived of proprioception after a viral infection, have largely demonstrated their inability to coordinate their actions. As this typically results in an inability to stand and walk, we focus here on the ability of deafferented patients to control their upper-limb movements. We will first present studies that provided striking evidence for the role of proprioception in movement coordination before presenting our recent work on the role of proprioception in motor learning and how the loss of large somatosensory fibres may affect visual perception. http://dx. After amputation, the cortical regions of which the neuronal activity was related to the control of the missing limb will gradually be active in relation to another, generally adjacent, part of the body. This reorganization often goes together with a vivid perception of the presence of the missing limb, called "phantom limb". A little known phenomenon, but experienced by many amputees, is that the phantom limb can be moved at will. The patients feel the movements to be made in correspondence with their will and they are able to copy with their intact limb the movement they "performed" with their phantom limb. Results of recent studies suggest that, despite the cortical reorganisation, M1 still can send motor commands to the missing limb. These motor commands, being unable to project on the missing limb muscles, project on the preserved muscles of the stump, resulting in specific muscle activation patterns. We will (1) show the large panel of phantom movements experienced by patients and (2) make a comparison between the EMG patterns evoked by phantom movements and those generated by the patients for the control of myoelectric prostheses. Funding: Project financed by the Region Provence-Alpes-Cote d'Azur (Projet ExplorAmp, 2012) and CNRS (DEFISENS, 2013).

Human Muscle Spindles Act as Forward Sensory Models

Modern theories of motor control incorporate forward models that combine sensory information and motor commands to predict future sensory states. Such models circumvent unavoidable neural delays associated with on-line feedback control. Here we show that signals in human muscle spindle afferents during unconstrained wrist and finger movements predict future kinematic states of their parent muscle. Specifically, we show that the discharges of type Ia afferents are best correlated with the velocity of length changes in their parent muscles approximately 100-160 ms in the future and that their discharges vary depending on motor sequences in a way that cannot be explained by the state of their parent muscle alone. We therefore conclude that muscle spindles can act as "forward sensory models": they are affected both by the current state of their parent muscle and by efferent (fusimotor) control, and their discharges represent future kinematic states. If this conjecture is correct, then sensorimotor learning implies learning how to control not only the skeletal muscles but also the fusimotor system.

The rubber hand illusion in action

In the well-known rubber hand illusion (RHI), watching a rubber hand being stroked while one's own unseen hand is synchronously stroked, induces a relocation of the sensed position of one's own hand towards the rubber hand [Botvinick, M., & Cohen, J. (1998). Rubber hands ‘feel’ touch that eyes see. Nature, 391(6669), 756]. As one has lost the veridical location of one's hand, one should not be able to correctly guide one's hand movements. An accurate representation of the location of body parts is indeed a necessary pre-requisite for any correct motor command [Graziano, M. S. A., & Botvinick, M. M. (1999). How the brain represents the body: Insights from neurophysiology and psychology. In D. Gopher, & A. Koriat (Eds.), Attention and performance XVII—Cognitive regulation of performance interaction of theory and application (pp. 136–157)]. However, it has not yet been investigated whether action is indeed affected by the proprioceptive drift towards the rubber hand, nor has the resistance of visual capture in the RHI to new proprioceptive information been assessed. In the present two kinematic experiments, we show for the first time that action resists the RHI and that the RHI resists action. In other words, we show a dissociation between illusion-insensitive ballistic motor responses and illusion-sensitive perceptual bodily judgments. Moreover, the stimulated hand was judged closer to the rubber hand for the perceptual responses, even after active movements. This challenges the view that any proprioceptive update through active movement of the stimulated hand erases the illusion. These results expand the knowledge about representations of the body in the healthy brain, and are in line with the currently most used dissociation between two types of body representations so far mainly based on neuropsychological patients [Paillard, J. (1991). Knowing where and knowing how to get there. In J. Paillard (Ed.), Brain and space (pp. 461–481); Paillard, J. (1999). Body schema and body image: A double dissociation in deafferented patients. In G. N. Gantchev, S. Mori, & J.Massion (Eds.), Motor control, today and tomorrow (pp. 197–214)].

Preserved and Impaired Aspects of Feed-Forward Grip Force Control After Chronic Somatosensory Deafferentation

Background. Although feed-forward mechanisms of grip force control are a prerequisite for skilled object manipulation, somatosensory feedback is essential to acquire, maintain, and adapt these mechanisms. Objective. Individuals with complete peripheral deafferentation provide the unique opportunity to study the function of the motor system deprived of somatosensory feedback. Methods. Two individuals (GL and IW) with complete chronic deafferentation of the trunk and limbs were tested during cyclic vertical movements of a hand-held object. Such movements induce oscillating loads that are typically anticipated by parallel modulations of the grip force. Load magnitude was altered by varying either the movement frequency or object weight. Results. GL and IW employed excessive grip forces probably reflecting a compensatory mechanism. Despite this overall force increase, both deafferented participants adjusted their grip force level according to the load magnitude, indicating preserved scaling of the background grip force to physical demands. The dynamic modulation of the grip force with the load force was largely absent in GL, whereas in IW only slower movements were clearly affected. Conclusions. The authors hypothesize that the deafferented patients may have utilized visual and vestibular cues and/or an efferent copy of the motor command of the arm movement to scale the grip force level. Severely impaired grip force-load coupling in GL suggests that sensory information is important for maintaining a precise internal model of dynamic grip force control. However, comparably better performance in IW argues for the possibility that alternative cues can be used to trigger a residual internal model.

Differential effects of cortical lesions in humans.

The best-known example of motor deficits after cortical lesions is contralateral paresis and spasticity after damage to the precentral motor strip. After recovery the residual motor functions can be used in a purposive and skillful manner. In patients with lesions of the supplementary motor area (SMA) and cingulate gyrus transient akinesia and mutism have been described. Lesions restricted to more lateral parts of the premotor field interfere with proximal muscle function and interlimb coordination, whereas distal motor activity and bimanual coordination are unimpaired. In contrast, hand function in patients with parietal lesions is severely disturbed. This dysfunction includes deficits such as ataxia, dysmetria and postural instability that are typically observed in deafferented patients. Severe disturbances of the purposive behaviour of the hand during exploratory finger movements and manipulation of objects are seen in patients with posterior parietal lesions. Observations in human patients are compatible with the hypothesis that lesions of the frontal agranular motor fields interfere with the control of postural and force control whereas parietal lesions are associated with motor programme disorders affecting the use of the hand or the eye as a sense organ or affecting more complex motor behaviour.

Bimanual circling in deafferented patients: Evidence for a role of visual forward models

The present study investigated the role of ideation and visual feedback, and their interaction in movement control in the absence of somatosensory feedback, with the hypothesis that visual imagery and internal visual models may play a crucial role in performance even without feedback. Two chronically deafferented participants, GL and IW, circled bimanually two occluded cranks first without vision and then with hand-congruent and hand-incongruent visual feedback provided by visible flags. Without vision, GL was unable to circle the cranks. In contrast, IW performed spontaneously a symmetric pattern. Again without feedback, IW performed an instructed symmetric crank pattern well, but was unable to perform anti-phase cranking. With hand-congruent visual feedback, GL and IW were able to perform both symmetric and anti-phase movements, with symmetry being more accurate. Visual feedback during preceding trials made possible trials without visual feedback in GL and improved anti-phase trials in IW. Frequency-transformed incongruent visual feedback resulted in poor performance in part due to unsuitable hand-related strategies. However, IW improved in the latter task after detailed explanations of the condition. In conclusion, we suggest that both participants use visual imagery and visual forward models to control their hand movements. Visual updating of the forward model also improves performance with no vision. In addition, IW seemed to have been able to move from a focus on hand position to one on the transformed visual feedback to improve movement control in the incongruent feedback/movement condition.

Ghost buster: The reality of one’s own body

What are the epistemic bases of the knowledge of the reality of our own body? Proprioception plays a primordial role in body representation and more particularly at the level of body schema. Without proprioception people can feel amputated and the mislocalization of proprioceptive information through the remapping of the Penfield Homonculus induces illusions of phantom limbs, illusions that contradictory visual feedback cannot erase. However, it turns out that it is not as simple as that and that vision also intervenes in body knowledge: vision of one’s own body allows deafferented patients to move and phantom limbs to disappear. Finally, the existence of phantom limbs in aplasic patients as well as studies on neonates provide evidence of an innate component of body representation.

Visual proprioception in the timing of movements: evidence from deafferentation

The present study investigated the control of movements in two patients with severe somatosensory deafferentation by systematically manipulating the visual information about the produced movements. In a synchronization task requiring the production of finger taps in synchrony with a regular auditory signal, participants controlled their movements under full vision or when the sight of the effector was partially or completely occluded. Results demonstrated large effects of visual feedback on the synchronization performance in the deafferented patients. Although the patients' performance differed substantially from that of unimpaired controls under partial or no feedback, their performance was comparable under full vision, the latter suggesting a compensation of the somatosensory loss by visual monitoring.

The effect of sensory feedback on the timing of movements: Evidence from deafferented patients

The role of sensory feedback in the control of movements was investigated in two deafferented patients with complete loss of cutaneous touch and movement/position sense below the neck and two control groups of different ages. In a synchronized repetitive finger-tapping task in time with a regular auditory pacing signal, the deafferented participants showed a strong influence of extrinsic feedback. In contrast to controls who demonstrated a typical asynchrony between their taps and the pacing signal in all feedback conditions, the deafferented participants, with auditory feedback and visual monitoring, showed no asynchrony between finger taps and the pacing signal. These findings support the view that sensory information plays a crucial role in the anticipatory timing of movements.

The contribution of proprioceptive feedback to sensorimotor adaptation

It is known that proprioceptive signals from muscles, joints, and skin are involved in the execution of aimed arm movements, but their role in the acquisition of new motor behaviour is largely unknown. Previous research using deafferented patients yielded inconsistent findings: sensorimotor adaptation was found to be less, equal, or even better than in controls. The present study uses a different approach: we degraded proprioceptive signals in healthy subjects by wrist vibration, while leaving them intact in a control group. In order to induce sensorimotor adaptation, both groups executed pointing movements under a visual (Exp. A) or a mechanical perturbation (Exp. B). We found that adaptation to the visual distortion was little affected by vibration, while adaptation to the mechanical distortion was substantially impaired. We conclude that proprioceptive signals which overtly disagree with visual ones (Exp. A) are not used for adaptation, while those which largely agree with visual ones (Exp. B) are used to enhance adaptive recalibration. These results indicate that intact proprioception is needed for mechanical but not for visual adaptation, which implies that the underlying mechanisms are at least partly distinct.

Right temporoparietal cortex activation during visuo-proprioceptive conflict.

The conflict between vision and proprioception has been proposed to explain why healthy subjects perform worse than proprioceptively deafferented patients in conditions with optical displacement, e.g. novel mirror drawing. It is not known which brain processes depend upon the successful integration of visual and proprioceptive information and are therefore impaired when these modalities disagree. With fMRI in healthy subjects we compared brain activity across two conditions with similar visual and proprioceptive stimulation and similar task demands that differed by the congruence of movement showed by the two modalities. Subjects felt the passive movement of the right index finger on a rectangular field and watched a cursor moving on a computer screen. Cursor and finger locations either mapped onto each other (congruent condition) or did not (incongruent condition). Monitoring incongruent compared with congruent movement activated the premotor area bilaterally and the right temporoparietal junction. These brain areas have previously been associated with shifts in the attended location in the visual space. These findings suggest an interaction between vision and proprioception in orienting to spatial locations.

Individual semicircular canal function in superior and inferior vestibular neuritis.

To examine the concept of selective superior and inferior vestibular nerve involvement in vestibular neuritis by studying the distribution of semicircular canal (SCC) involvement in such patients. Vestibular neuritis was traditionally thought to involve the superior and inferior vestibular nerves. Recent work suggests that in some patients, only the superior nerve is involved. So far there are no reported cases of selective involvement of the inferior vestibular nerve. The authors measured the vestibuloocular reflex from individual SCC at natural head accelerations using the head impulse test. The authors studied 33 patients with acute unilateral peripheral vestibulopathy, including 29 with classic vestibular neuritis and 4 with simultaneous ipsilateral hearing loss, 18 healthy subjects and 15 surgical unilateral vestibular deafferented patients. In patients with preserved hearing, eight had deficits in all three SCC, suggesting involvement of the superior and inferior vestibular nerves. Twenty-one had a lateral SCC deficit or a combined lateral and anterior SCC deficit consistent with selective involvement of the superior vestibular nerve. Two patients with ipsilateral hearing loss had normal caloric responses and an isolated posterior SCC deficit on impulsive testing. The authors propose that these two patients had a selective loss of inferior vestibular nerve function. Vestibular neuritis can affect the superior and inferior vestibular nerves together or can selectively affect the superior vestibular nerve.

Chapter 19 The cerebellum as a neuronal prosthesis machine

This chapter discusses the architecture of the cerebellar cortex, which represents a substrate that can be exploited for controlling skilled movements by a multi-electrode device. The idea may seem futuristic to some, hence, it is buoyed by a number of factors. A multi-electrode stimulation device interfaced to the cerebellum for modulating movement taps into the natural function of the cerebellum to modulate ongoing voluntary movement. Multi-neuron stimulation of visual cortex or the dorsal cochlear nucleus provides vision and audition to peripherally deafferented patients. Combinations of synchronous activation of olivocerebellar clusters provide inertial breaks and asynchronous fast activations to maintain or fine tune position that has to be utilized.

PET study of visually and non-visually guided finger movements in patients with severe pan-sensory neuropathies and healthy controls.

Although patients with sensory neuropathies and normal muscle power are rare, they have been extensively studied because they are a model for dissociating the sensory and motor components of movement. We have examined these patients to determine the cerebral functional anatomy of movement in the absence of proprioceptive input. In addition, the disabling symptoms of these patients can be substantially improved by visually monitoring their movements. We hypothesized that, during visually guided movements, these patients would show overactivity of regions specialized for visuomotor control with the possible additional involvement of areas that normally process somatosensory information. We used positron emission tomography (PET) and the tracer H(2)(15)O to determine the functional anatomy of visually and non-visually guided finger movements in three patients with long-standing pan-sensory neuropathies and normal muscle power and six healthy controls. Five conditions were performed with the right hand: a sequential finger movement task under visual guidance, the same motor task without observation of the hand, monitoring a video of the same sequential finger movement, a passive visual task observing a reversing checkerboard, and an unconstrained rest condition. Data were analyzed using conventional subtraction techniques with a statistical threshold of z>2.33 with corrections for multiple comparisons. When compared with the control group, activation was not deficient in any brain areas of the patient cohort in any of the contrasts tested. In particular, in the non-visually guided movement task, in which meaningful visual and proprioceptive input was absent, the patient group activated primary motor, premotor, and cerebellar regions. This suggests that these areas are involved in motor processing independent of sensory input. In all conditions involving visual observation of hand movements, there was highly significant overactivity of the left parietal operculum (SII) and right parieto-occipital cortex (PO) in the patient group. Recent non-human primate studies have suggested that the PO region contains a visual representation of hand movements. Overactivity of this area and the activation of SII by visual input appear to indicate that compensatory overactivity of visual areas and cross-modal plasticity of somatosensory areas occur in deafferented patients. These processes may underlie their ability to compensate for their proprioceptive deficits.

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 programmed, 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 degrees supination followed by a 20 degrees 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 deafferented patients, unaware of the procedure, always produced a 20 degrees 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.

Proprioceptive control of interjoint coordination.

This paper reviews a series of experiments comparing intact controls with functionally deafferented patients to determine the role of proprioception in controlling dynamic interactions between limb segments during movement. We examine the control of hand path in a planar movement-reversal task and in a familiar three-dimensional gesture with similar biomechanical characteristics. In the planar task subjects had to move their hand out and back along a series of straight-line segments in the horizontal plane without visual feedback. The lengths and directions of the target line segments were chosen to require different amounts of shoulder motion while requiring the same elbow excursion. In controls, hand paths were, as required, straight with sharp bends at the outermost point. In patients, however, distinctive errors appeared at movement reversals, consisting of widened hand paths resulting from desynchronization in the reversals of elbow and shoulder motions. These errors reflected an inability to program elbow muscle contractions in accord with interaction torques produced at the elbow by variations in acceleration of the shoulder. The reversal errors were substantially reduced after patients had practiced for a few trials while visually monitoring movements of their arm. The improvement was not limited to the direction where they had practiced with vision, but also extended to other directions in which the elbow torques were different. This suggests that practice with vision of the arm served to improve the general rules that subjects used to plan movement, rather than simply improving the performance of a specific response. Similar to their performance on the planar task, the patients made errors in interjoint coordination during unconstrained three-dimensional gestures with movement reversals. We conclude (i) that both the planning and the learning of movement required an internal model of the dynamic properties of the limb that takes account of interaction torques acting at different joints; (ii) that this internal model is normally established and updated using proprioceptive information; but (iii) that when proprioception is lacking, vision of the limb in motion partially substitutes for proprioception.

Orienting of attention in deafferented patients

Visual attentional processes were compared in two deafferented patients and 11 normal subjects. Two consecutive stimuli were presented in rapid succession in one of two locations. A peripheral cue first oriented attention to one location where a response was requested. After 100 msec, a second response was required at either the same or opposite location (valid vs invalid cue). Four probabilities of valid cue occurrence were presented: 100, 80, 50 and 20%. Results showed (1) faster reaction times for the second response on cued than on uncued signals; (2) greater attentional effects with increased cue probability; (3) smaller attentional effects in patients. These findings suggest that the patients adopted a cost-minimizing strategy.

The role of sensory information in the guidance of voluntary movement: reflections on a symposium held at the 22nd annual meeting of the Society for Neuroscience.

This article reviews a symposium on the sensory control of movement held at the 22nd annual meeting of the Society for Neuroscience. Four speakers addressed a large audience on the proposition that "one can only control what one senses." Charles Vierck supported the notion with a description of the severe motor deficits caused by lesions of the spinal dorsal columns (DCs) in monkeys. In the discussion of Vierck's presentation, Robert Forget described the difficulties experienced by deafferented patients in tasks of daily life. Next, John Brooke showed that sensorimotor transformations vary greatly with task, anticipation, and uncertainty. In light of this, he questioned the simplifications inherent in servo and equilibrium-point theories of motor control. Paul Cordo then showed that in a rapid throwing task, proprioceptive information is used to control the moment of release (contradicting the idea that sensory feedback is too delayed for ballistic movements). Dick Burgess, like Brooke, criticized equilibrium-point models; he argued that a subject's sense of effort is a measure of the internal motor command, which should correspond to specific equilibrium points. However, his experimental data were inconsistent with this interpretation. He suggested instead that motor output is adjusted by comparing incoming afferent information to an expected "afferent template." Anatol Feldman and Mark Latash disagreed, saying that a constant sense of effort does not imply a constant equilibrium-point command. The equilibrium-point debate was not resolved, but the symposium ended with a consensus that in most motor tasks, one can control only what one senses.