Illusion of arm movement evoked by tendon vibration in patients with spinal cord injury

Abstract

Background: Studies in healthy people show that stimulation of muscle spindles through frequency-specific tendon vibration (TV) induces the illusory perception of movement. Following spinal cord injury (SCI), motor and sensory connections between the brain and parts of the body below-the-lesion level are partially or totally impaired.

Objective: The present investigation is a descriptive study aimed to investigate whether people living with SCI may experience movement illusions comparable to a control group.

Methods: Healthy and people with SCI were asked to report on three illusion-related features (Vividness, Duration, Illusory Extension) after receiving 70 Hz TV on the biceps brachii tendon of both arms. Two different forces of stimulation were applied: 2.4 N and 4.2 N.

Results: Both patients and controls were susceptible to the kinesthetic illusion. However patients presented lower sensitivity to TV than healthy subjects. Participants rated stronger illusions of movement after 4.2 N than 2.4 N stimulation in all the three illusion-related features. Further, patients reported atypical illusory experiences of movement (e.g. as if the arm wanted to extend, or a sensation of pushing against something) that may reflect different reorganization processes following spinal cord injury.

Conclusion: The study provides a preliminary evidence of the possible use of the proprioceptive stimulation in the upper limbs of people living with SCI. Results are discussed in the light of recent advancements of brain-computer applications based on motor imagery for the control of neuroprosthetic and robotic devices in patients with severe sensorimotor deficits.

Keywords

Spinal cord injury tendon vibration illusion of movement spinal cord rehabilitation proprioception

1 Introduction

People who suffer from a spinal cord injury (SCI) exhibit different impairments of the sensorimotor function (Silva et al., 2014) that dramatically impact quality of life and limits the interaction with the environment (Rognoni et al., 2014). The sensorimotor disconnection between the brain and body parts below the lesion level represents a challenge for rehabilitation protocols and the development of Brain Computer Interfaces (BCI) as they attempt to improve the control of robots and neuroprosthetic devices that may be suited for motor- and neuro-rehabilitation (Millán et al., 2014).

In this context, through the mechanical stimulation applied on tendons of different muscles, it is possible to intervene in the communication between afferent pathways and the brain. Focal tendon vibration (TV) can increase the frequency rate discharge of the muscle spindle primary endings (Roll et al., 1989; Tsay et al., 2015), altering the perceived position of the stimulated body part and eliciting a proprioceptive illusion of movement (Goodwin et al., 1972; Naito et al., 1999; Tidoni et al., 2015a) even during anaesthesia (Hellsing et al., 1978). Importantly, after the interruption of the tendon stimulation, the muscle spindles return to their pre-perturbation state, thus decreasing the rate discharge and generating a rapid opposite directional perception of illusory movement: a corollary post-vibration effect called aftereffect (Seizova-Cajic et al., 2007).

This technique might improve the use of BCI systems based on motor imagery abilities (Yao et al., 2015). Indeed, illusory movement following TV activates a fronto-parietal network (Naito et al., 1999; Amemiya & Naito 2016) and BCI performances are positively related to grey matter volume of premotor areas (Kasahara et al., 2015). Moreover, recent studies in healthy people used TV with virtual reality (VR) scenarios as a possible tool for post-stroke hand rehabilitation (Rinderknecht et al., 2013) and to better control of virtual upper-limb movements using a motor imagery-BCI system (Leonardis et al., 2012).

Although several parameters of TV (e.g. temporal duration and resolution; Seizova-Cajic et al., 2007; Fuentes et al., 2012) and illusion features (e.g. direction, speed and movement trajectory; Casini et al., 2008; Thyrion et al., 2009; Roll et al., 2009) have been investigated, little is known about the role of the applied force of the vibration in regulating the illusory movement perception.

Cordo and colleagues (1993) recorded the responsiveness of muscle afferents in a sample of healthy subjects by vibrating the tibialis anterior tendon at different frequencies and averaged forces. The results showed an increment of muscle spindles sensitivity to TV by increasing the vibration force. Moreover, Ribot-Ciscar and colleagues (2003) applied TV on the biceps and triceps tendons of 8 patients characterized by a cervical injury to investigate the effect of the stimulation on muscles contraction. In this study the illusory extension of the arm varied depending on the stimulation setup. When the arm was slightly extended and supported by an experimenter all people with SCI reported the illusory experience. Contrary when the TV was applied with the upper limb inside the setup (with the elbow flexed to 90°) only three people with SCI felt an illusory extension of the arm and just for the 27% of the trials. To date no evaluations of the illusory movements were reported.

The present study aims to describe the subjective perception of the movement illusions and the effect of the vibration force on the biceps tendons in a sample of healthy and people living with SCI. This explorative and descriptive investigation may likely provide exploitable information for the improvement of BCI systems that use TV as a tool for sensory feedback (Yao et al., 2015, Leonardis et al., 2012, Ramos-Murguialday et al., 2012).

2 Material and methods

2.1 Participants

Data was collected from 16 people affected by spinal cord injury (5 females, mean ± s.e.m., age 43.25±3.83). Importantly, two patients were discarded from the main sample (Patient A and Patient B; see Table 1 and Section 3.1) due to the impossibility of starting the experimental session. Answers from Patient C were not collected due to technical failure. Thus, the final sample was of 13 people with SCI (4 females, age 39.77±4.13) and 13 healthy control subjects (4 females, age 39.38±3.80). Patients were screened and selected for participation both at the IRCCS Fondazione Santa Lucia and the Unipolar Unit of the Andrea Alesini Hospital, both located in Rome (Italy). Patients had different cervical spinal cord lesions with traumatic or non-traumatic origin and the time since lesion onset ranged from 17 to 636 months (138.08±46.58). According to the ASIA Impairment Scale (AIS; Kirshblum et al., 2011), the completeness of the lesion is defined on the basis of sensory and motor preservation of the lower sacral segments (see Table 1). Due to the variable onset of the spinal lesion patients were asked to verbally report their manual preference before and after injury (see Table 1). The same approach was adopted for control participants (12 right-handed, 1 left-handed).

Participants had normal or corrected-to normal vision with an absence of brain damage, psychiatric or neurological diseases. Each participant gave written informed consent after receiving explanation of the experimental procedure. The study protocol was approved by the ethics committee of the Fondazione Santa Lucia in accordance with the ethical standards of the Declaration of Helsinki.

2.2 Vividness Motor Imagery Questionnaire (VMIQ)

Motor imagery may change the effect of TV in modulating the illusory extension/flexion of the arm (Kitada et al., 2002; Thyron et al., 2009; Shibata et al., 2013). Thus, given the possible link between the ability to imagine motor actions and the perception of illusory movements, we measured imagery abilities using the Vividness Motor Imagery Questionnaire (VMIQ; Isaac et al., 1986; see also Roberts et al., 2008). This questionnaire has been used to compare the capacity of healthy participants (Alkadhi et al., 2005; Neuper et al., 2009) and people with sensorimotor diseases to imagine actions (Hotz-Boendermaker et al., 2008; Ionta et al., 2016). Participants rated the vividness associated to the imagery of 24 actions using a 1-to-5 point Likert scale (1 = excellent imagination of the movement performance, as lively as actual performance, 5 = no image at all). In two separate sessions participants were asked to imagine and evaluate, with closed eyes, the kinesthetic sensations associated with a specific movement, adopting a first-person perspective (kinesthetic subscale, “Imagine in a first-person perspective, the kinesthetic sensation associated with the given movement.”) or a third-person perspective (visual subscale, “Imagine that someone else is executing the movements.”). The order of first and third person perspectives (kinesthetic and visual subscale respectively) was balanced across participants. Questionnaire scores ranged from 24 to 120, with 24 representing the highest vividness score. That is, the lower the score, the more vivid was the imagery. To avoid order effects, the items were delivered randomly.

2.3 Proprioceptive stimulator

The proprioceptive stimulation system was composed of a set of supports and an actuator with adjustable position and orientation (see Fig. 1; see also for details Leonardis et al., 2012; Tidoni et al., 2015a). A hemispherical tactor (15 mm diameter), mounted at the tip of the actuated moving shaft, was in contact with the skin. The modulation of the vibrating stimulus force and frequency was controlled by embedded electronics interfaced with a host PC running XVR software (XVR media, Carrozzino et al., 2005). Importantly, the force on the moving shaft could be modulated independently from the frequency of the vibration (Leonardis et al., 2012).

2.4 Procedure and apparatus

Participants were seated in front of a table close to the proprioceptive device and invited to assume a comfortable and upright position. Following the motor imagery evaluation, subjects underwent the proprioceptive assessment and the experimental phase for each arm in two separate sessions.

2.4.1 Proprioceptive assessment

Participants’ elbows were gently placed inside the proprioceptive stimulator. The proprioceptive device allowed to place the arms in a stable and comfortable manner with an elbow angular position of approximately 120°. The plastic skin tactor was positioned over the corresponding tendon. Subjects were asked to relax, close their eyes and focus on any possible change in the perception of their upper limb during the stimulation. Participants were informed that the stimulation might change the perceptive experience of their arm. No information about the direction of such change was provided (e.g. extension, flexion, right or left translation) in order to avoid expectancy or biased effects.

During the proprioceptive assessment phase a mechanical vibration of 40 Hz was applied with a force of 2.4 N for 30 seconds. These parameters have been used to elicit a clear illusion of movement (Tidoni et al., 2015a) with the adopted device. After the vibration, participants were invited to freely describe the perceived sensation. This procedure assisted in finding the optimal position to elicit an illusory sensation related to the proprioceptive stimulation and familiarized participants with the device and the illusory experience.

2.4.2 Experimental session

Force and frequency were selected based on previous studies (Leonardis et al., 2012; Tidoni et al., 2015a). To avoid any ceiling effect we stimulated with a constant frequency of 70 Hz that is close to the optimum for generating the illusion with this stimulator (Naito et al., 1999; Tidoni et al., 2015a). Moreover, in order to generate a clear subjective change in the perceived vibratory force and to avoid any possible discomfort, the vibrating stimulus was generated applying two sinusoidal forces of 2.4 N (based on Tidoni et al., 2015a) and 4.2 N (75% higher relative to 2.4 N and close to the force applied by Leonardis et al., 2012). This procedure ensured a strong but not annoying pressure of the tendons and revealed to be successful in eliciting a higher illusory experience when a force of 4.2 N relative to 2.4 N was applied (see Results).

The experimental session was composed of two separate blocks in which both arms were stimulated. Each block included three trials per applied force and each trial lasted 60 s characterized by the first 15 s of stimulation and the remaining 45 s for answering the illusory evaluation and rest (for a total of six stimulation per arm, 3 trials at 2.4 N and 3 trials at 4.2 N). Stimulated arm and blocks order were balanced across subjects. The device guaranteed a stationary position of the arms and no overt limb movements were detected by the experimenter. Finally, in order to prevent subjects being distracted by the sound of vibrations or other external sources, white noise was provided through a set of headphones.

Participants, with eyes closed and in a relaxed position, received tendon vibration and were then asked to rate the Vividness, Duration and Extension (Naito et al., 1999; Tidoni et al., 2015a) of the illusory movement by choosing a numerical value on a 0–100 scale. Vividness referred to the intensity of illusory perception (0 = did not move at all; 100 = as vivid as a real movement), Duration assessed the illusion lasting throughout the vibration (0 = never started; 100 = as long as the stimulation), Extension was the amount of perceived arm displacement generated by stimulation (0 = stationary; 100 = reached the maximum extension). Illusory movement was considered to be any action-related perception referred to the stimulated arm during the vibration of thetendon.

Mean scores for each illusory feature were treated as dependent variables and analysed using a mixed 2×2×2 factorial design with Group (patients, controls) as the between-subject factor, and stimulated Arm (left, right) and applied Force (2.4 N, 4.2 N) as within-subject factors. All significant main effects and interactions were analysed by means of Newman-Keuls Post hoc. Normality of skewness and kurtosis were checked between ±1.96 (all z-scores were within ±1.96; Field, 2013).

3 Results

3.1 Motor imagery

Patients and controls were comparable in their ability to imagine motor actions from a first and third person perspective (kinesthetic subscale: Patients = 55.46±5.64, Controls = 49.08±7.02; t₍₂₄₎ = 0.71, p = 0.49, r = 0.14; visual subscale: Patients = 48.08±5.87, Controls = 49.69±7.07; t₍₂₄₎ = 0.18, p = 0.86, r = 0.04). Thus the two groups were similar in motor imageries reducing the impact this may have had on subjective experience of illusory movement perception (Kitada et al., 2002; Shibata & Kaneko 2013).

3.2 Vividness

A main effect was found for Arm (F_(1,24) = 5.71, p = 0.025, η_p² = 0.192) with higher vividness during the stimulation of the left arm (66.70±5.53) relative to the right arm (58.87±6.52). Moreover, the main effect of applied Force was significant (F_(1,24) = 26.25, p < 0.001, η_p² = 0.552), indicating that the illusory movement was perceived as more vivid at 4.2 N (70.52±5.94) rather than 2.4 N (55.06±6.08; see Fig. 2a). Finally, there was a trend of the group (F_(1,24) = 3.81, p = 0.062, η_p² = 0.137) that was accounted for by less vivid perception of illusory movement in SCI (52.01±10.14; patients with A.I.S. grade A, 31.46±10.29; patients with A.I.S. grade B-C-D, 69.62±13.94) than in controls (73.57±4.37; see Fig. 2b). No other effects were found (all F_(1,24) < 2.87, p > 0.103, η_p² < 0.107).

3.3 Duration

A main effect of Force emerged from analysis (F_(1,24) = 16.52, p < 0.001, η_p² = 0.408), revealing that perception of the illusion lasted longer when participants received stimulation at 4.2 N (63.79±5.68) rather than at 2.4 N (52.64±5.87; see Fig. 2a). An interaction between Group and Arm (F_(1,24) = 4.87, p = 0.037, η_p² = 0.169) was found. This is accounted for by the fact that SCI patients reported a shorter illusory movement during the vibration of the right tendon (42.44±10.72; A.I.S. grade A, 24.86±12.66; patients with A.I.S. grade B-C-D, 57.50±15.18) compared to left (54.81±9.70; p = 0.015; A.I.S. grade A, 40.83±11.83; A.I.S. grade B-C-D, 66.79±14.06). Controls did not differ in this illusory feature between the right and left stimulation (Right Arm, 69.01±4.98; Left Arm, 66.60±4.56; p = 0.616) and no further differences between groups were noticed (all p > 0.099). All other main effects and interactions were not significant (F_(1,24) < 3.56, p > 0.071, η_p² < 0.129).

3.4 Extension

A main effect was found for Force (F_(1,24) = 28.67, p < 0.001, η_p² = 0.544), with higher reports of illusory extension at 4.2 N (64.45±6.27) rather than at 2.4 N (46.44±5.39). A significant effect was found for Group (F_(1,24) = 5.69, p = 0.025, η_p² = 0.192), revealing a reduced sensitivity to the illusory extension for people with spinal cord injury (43.17±9.41; A.I.S. grade A, 29.04±14.34; A.I.S. grade B-C-D, 55.27±11.37) relative to Controls (67.72±4.17; see Fig. 2c).

Finally, we explored the contribution of motor imagery (patients and controls) and time since injury (patients only) in the illusory movement perception by means of three correlational analysis. For each subject the mean score of the illusion related questions (Vividness, Duration and Extension) was computed and a general index (G-index) of participant’s sensitivity to the illusory experience was calculated collapsing the scores of the three features. No correlations between the G-index and the kinesthetic subscale (Patients: r = 0.20, p = 0.52; Controls: r = 0.12, p = 0.71) and between the G-index and time since injury (Patients: r = 0.00, p = 0.99) were found (see Movement Illusion and Spinal Cord Injury Section in the Discussion below).

4 Discussion

The present study aimed to investigate the illusion of movement induced by tendon vibration (TV) in people with spinal cord injury (SCI). A sample of tetraplegic patients were selected to compare their illusory experience with a matched sample of healthy subjects. TV was applied on the biceps brachii tendons of both arms with a constant 70 Hz stimulation and the results showed that both 2.4 N and 4.2 N stimulation forces were able to generate a sensation of arm extension. Crucially, participants rated higher vividness, duration and illusory arm extension after receiving TV with a force of 4.2 N rather than 2.4 N. Moreover, eight patients reported the classic illusory perception (a downward extension of the stimulated arm), whilst others reported an altered feeling of movement during the vibratory stimulation (e.g. pins and needles; see Table 2 and Section 4.3 for schematic and detailed report of patients, respectively).

4.1 Bodily illusion in spinal cord injury

The pathophysiological variability of people living with SCI and their individual recovery paths (Fawcett et al., 2007) may activate different reorganization processes that regulate the link between brain and body following a deafferentation. Recently, an illusory sensation of owning two additional pairs of legs located medially to his real legs was reported in a 43-year-old SCI patient with a complete lesion at C6 level (supernumerary phantom limb syndrome; Choi et al., 2013). The intensity of such illusions varied depending on body posture of the patient, being highest in supine position and lowest whilst sitting. According to the authors’ interpretation, this perception could be explained by the loss of afferent information due to sensory and proprioceptive impairment that ultimately caused alterations to the innate body image (Choi et al., 2013).

Moreover, recent studies of body illusions induced through a rubber hand (Rubber Hand Illusion, RHI; Botvinick & Cohen 1998), show in patients with spinal cord injury different patterns of subjective reports and proprioceptive drift (an index that measures the illusory distance experienced between the false and real hands) depending on the lesion level. In Lenggenhager et al. (2012) for instance, the authors induced RHI in three separate groups: healthy, paraplegic and tetraplegic. It was found that while all healthy and paraplegic participants were able to perceive the illusion, just half of the tetraplegic group experienced the ownership of a false hand. Interestingly, proprioceptive drifts were reported by the healthy and by half of the tetraplegic group, but not by the paraplegics. Disparate results were found in another study (Scandola et al., 2014) which used the same participant categories to demonstrate a possible face-hand remapping process following SCI. However only the healthy group perceived illusory drifts of their real hand and only the tetraplegic group experienced higher levels of illusory ownership when their face was stimulated (Scandola et al., 2014). Further, a single case study (Tidoni et al., 2014) reported a 30-year-old man with SCI equivalent to a complete lesion (C4, AIS A), who was able to perceive both the RHI and the proprioceptive drifts of his hand, even when another part of the body (the cheek) was stimulated.

In the present study patients reported atypical illusory experiences (see Section 4.3) suggesting anomalous processing of the vibratory stimulation. Overall, subjective reports during an illusory experience in people with SCI may hint that reorganization mechanisms and altered processing of sensorimotor information may have intervened after the injury.

4.2 Movement illusion and spinal cord injury

Recent studies reported how several vibration parameters are relevant to induce the experience of movement illusion in healthy subjects (Cordo et al., 1993; Fuentes et al., 2012; Schofield et al., 2015; Tidoni et al., 2015a). Nonetheless little is known about the perceptual experience of tendon vibration applied at different forces.

The present study, based on current knowledge, extends previous investigation on the role of the vibration force in healthy (Cordo et al., 1993) and illusory movement perception in a sample of people affected by sensorimotor disconnection (Ribot-Ciscar et al., 2003) showing that higher forces increase the perceived illusory movement both in people living with SCI and controls. In particular, Cordo and colleagues (1993) applied TV over the tibialis anterior tendon and tested the corresponding responsiveness of muscle afferent trough microneurographic techniques. Varying the applied force (from 0 N to 3 N) and frequency (from 20 Hz to 110 Hz), results showed an increment of muscle spindle responsiveness by increasing the force and not thefrequency.

Patients felt a lower extension of arms and lower vividness of illusion as compared to healthy participants (Fig. 2c). Importantly, our groups did not differ in motor imagery abilities and did not reveal any relation between the ability to imagine motor actions and the illusory movement. Several studies have indicated that imaging movements during TV can modulate the illusory perception (Thyrion et al., 2009; Shibata et al., 2013) proposing an interaction between afferents input from muscle spindles and efferent input from the cortical areas during motor imagery. However, no relation between the kinaesthetic subscale and illusory perceptions was observed suggesting that interactions between afferent and efferent signals may occur if motor imagery is performed during the proprioceptive stimulation (in our paradigm motor imagery was assessed before TV). Indirect evidence supporting this suggestion comes from a recent BCI study where concomitant motor imagery and TV improved the control of a virtual arm through a motor imagery based BCI system (Leonardis et al., 2012). Finally, we cannot exclude that the patients group used different motor strategies to perform the imagery task (Fiori et al., 2014).

Recently Scandola and colleagues (2016) showed a difference between a large sample of people living with SCI and healthy in imaging movements. In their study authors assessed motor imageries using a different questionnaire (VMIQ-2, Roberts et al., 2008) and observed a reduced ability to imagine motor actions in SCI people with cervical lesion (Scandola et al., 2016). The fact that motor imagery abilities between SCI people and controls differ depending on the adopted questionnaire (Scandola et al., 2016, Ionta et al., 2016) limits the possibility to draw strong conclusions based only on subjective reports and suggest that methodological and sample size differences may influence the results.

Moreover, patients and healthy participants perceived a more intense illusion of movement (Vividness) when they received stimulations on the left in respect to the right arm. Similarly, people living with SCI experienced a longer illusion (Duration) when the tendon vibration was applied on the left (non-dominant) compared to the right arm (dominant). The handedness of patients was mainly right lateralized, remaining largely unchanged from before-to-after injury, with the exception of one subject who passed from right to left preference and two patients who reported to be ambidextrous(Table 1).

Sensitivity to illusory movement can be influenced by handedness. In this regard, it was reported that both left-and right-handed healthy people tend to perceive a more vivid illusory movement after receiving stimulation on the non-dominant arm (Tidoni et al., 2015a), therefore suggesting a lateralized specialization of proprioception (Goble et al., 2008; Adamo & Martin 2009; Adamo et al., 2012). The present study confirms this result in part. Indeed, the lack of asymmetry in the duration for healthy participants and in the illusory extension for both groups may be linked with the different parameters used for TV. In Tidoni et al. (2015a) participants showed a preference for the non-dominant arm when stimulated at their best frequency (the frequency that elicited the highest illusory experience selected among a 40–120 Hz range in 20 Hz step) with a constant force of 2.4 N. Conversely, in the current study we manipulated the strength of vibration (2.4 N and 4.2 N) maintaining fixed the frequency at a 70 Hz. Thus, these different methodological aspects (subject-specific stimulation frequency and applied force) and the higher variability in SCI sample might explain the absence of asymmetry in the currentstudy.

4.3 Free reports of SCI patients in perceiving the illusion of movement

This section describes different sensations of movement as reported by the patients, (see Table 2 for a schematic summary of the variability of illusion).

4.3.1 Patient 2

After vibration of the left arm he reported feeling “as if my hand were pushing against the wall”. This sensation was independent from the applied force. Patient 2 was asked to rate the illusory experience following the standard criteria of evaluation (see Procedure and apparatus) and the ratings were used for the main analysis. No aftereffect was spontaneously reported. Vibration on the right arm generated pins and needles sensations. No illusory movement was generated in the experimental phase and a score of “0” was stored and entered in the main analysis.

4.3.2 Patient 3

After the vibration of the left arm at 2.4 N the patient spontaneously reported, in one out of three trials, the aftereffect illusion “as if it [the arm] goes backward” and rated the vividness of this experience as “90” on a 0–100 scale. Importantly, when the left arm was stimulated at 4.2 N during the first trial, he perceived the sensation “as if it [the arm] tried to wriggle” and then during the last two trials he reported that “the arm laterally translated by 2–5 centimetres” while it was in fact still. However the vividness of these sensations was clear (mean rating of 88.33). The patient was not able to quantify any illusory extension on a 0–100 scale and thus the absence of illusory extensions was scored as “0”. No aftereffect of the left arm during 4.2 N stimulation was spontaneously reported. He described an aftereffect illusion at the end of all stimulation at 2.4 N of the right tendon and after stimulation at 4.2 N he felt once “as if the arm was moving against something”. We asked Patient 3 to rate this illusion and the ratings were entered in the main analysis.

4.3.3 Patient 8

He reported that during the left tendon vibration with 2.4 N “it was as if it [the left arm] was attempting to move but something hindered it”. During the stimulation of the right tendon at 2.4 N and 4.2 N no illusory movement was reported and the proprioceptive tactor was perceived “as if it were moving along the arm surface”.

4.3.4 Patient 10

During the proprioceptive assessment he reported an unspecified sensation over the head. He experienced a normal illusory movement sensation and spontaneously reported also the presence of the aftereffect at the end of allstimulations.

4.3.5 Patient 11

The patient in one trial reported the sensation “as if the arm wanted to extend” during the stimulation of the right tendon at 4.2 N. The patient was asked to rate this sensation and the rating was entered in the main analysis.

4.3.6 Patient 12

In one trial during right arm stimulation at 2.4 N she reported a sensation “as if someone was strongly holding my elbow with their hand”.

4.3.7 Patient A

There were constraints in positioning the proprioceptive stimulator over the patient’s tendons due to the patient’s muscle rigidity. After some attempts to perform proprioceptive stimulation it was decided not to proceed with the experimental sessions. Importantly, in some trials he reported pins and needles on the left hand whenever the vibration was applied over the right and left tendon. He reported pins and needles on the right hand only in one right tendon stimulation trial.

4.3.8 Patient B

During the proprioceptive assessment the patient asked to stop after a few seconds of stimulation, reporting a painful sensation in her lower limbs described as “shocks that come from the bottom of the body”. As soon as the vibration was interrupted, the patient reported the physical discomfort ceased. It was decided not to further proceed with the experimental sessions.

4.3.9 Patient C

Due to technical failure the answers to the three illusory features were not stored on the host PC. He felt both in the left arm with 2.4 N and 4.2 N vibrations and in the right arm at 2.4 N a sensation “as if the arm remained in a fixed position while the whole body was moving backwards”.

4.4 Limitations of the current study

Some limitations of the study deserve a discussion. In this descriptive investigation we used subjective reports to study the effect of the vibratory force on the kinaesthetic illusory perception in a sample characterized by different spinal cord injuries. The relatively small and heterogeneous sample (i.e. lesion completeness and lesion level) may explain the variability of illusory movement perception in people who live with SCI and may have limited the possibility to find a correlation between the illusion and the SCI clinical data. Previous studies showed that TV can induce illusory experience in anesthetized body parts (Hellsing et al., 1978; Goodwin et al., 1972) and further studies are required to evaluate in detail the bottom-up processes and the mechanisms associated with such illusory experience in people with SCI following peripheral tendon stimulation. Moreover, we adopted only two forces to generate a clear perceptual change and the activity in the vibrated and antagonist muscle was not measured through electromyography (Ribot-Ciscar et al., 2003). Further studies are needed to assess the small increase in the applied force necessary to elicit a perceptual change in the illusory experience in healthy and people living with SCI and the amount of spared motor efference, as well sensory and proprioceptive afferences that may affect the quality of the illusion.

5 Conclusion

We investigated the illusion of movement induced by TV in people living with SCI. An illusory arm extension was elicited manipulating the vibratory force administered over the stimulated tendon. The force applied to the tendon increased the perceived illusory movement with higher vividness, duration and illusory arm extension after receiving TV with a force of 4.2 N rather than 2.4 N.

Recent studies suggested that bodily illusions may improve somatosensation in people living with SCI (Lenggenhager et al., 2013; Pazzaglia et al., 2016). Yet, how transient changes may become permanent is far to be fully understood. Moreover, advances in robotic and computer engineering allow for the development of novel interfaces and prostheses that could help people with sensorimotor impairments to interact once more with the environment (Millán et al., 2014). Thus, tendon vibration might provide the opportunity to exploit proprioceptive afferents for improving the control of these systems by means of motor imagery based BCI interfaces (Yao et al., 2015; Leonardis et al., 2012; Ramos-Murguialday et al., 2012; Galán et al., 2015; Hanakawa, 2015). Yet, the atypical illusory sensations reported by patients may represent a challenging aspect for building adaptable interfaces (Tidoni et al., 2015b) with a congruent feedback between visual and proprioceptive information.

Despite the mentioned limitations, our stimulation protocol was successful to observe some preliminary difference in movement illusion between the people living with SCI and controls. Finally, free reports hint at further investigations combining proprioceptive stimulation with visual information in order to generate a congruent visual feedback that may be useful for BCI applications based on motor imagery (Leonardis et al., 2012, Ramos-Murguialday et al., 2012, Yao et al, 2015; Tidoni et al., 2015b).

Conflict of interest statement

The Author(s) declare(s) that there is no conflict of interest.

Footnotes

Acknowledgments

Funded by the EU Information and Communication Technologies Grant (VERE project, FP7-ICT-2009-5, Prot. num. 257695), the Italian Ministry of Health (RF-2010-2312912) to SMA and the BIAL Foundation (Prot. num. 2014/150)to ET.

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