Abi Chebel

Nadège A Roussillon

Christophe Bourdin

Pascale Chavet

Fabrice R Sarlegna
email: fabrice.sarlegna@univ-amu.fr

Najib M Abi Chebel

Joint Specificity and Lateralization of Upper-Limb Proprioceptive Perception

Keywords:

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Introduction

Perceiving where are our own body segments is a key element in everyday life. Such perception partly relies on proprioception, the sense of position and movement of body segments based on receptors in the muscles, tendons, joints, and skin [START_REF] Cole | Losing touch: A man without his body[END_REF][START_REF] Elangovan | Assessing Proprioceptive Function: Evaluating Joint Position Matching Methods Against Psychophysical Thresholds[END_REF][START_REF] Fuentes | Where is your arm? Variations in proprioception across space and tasks[END_REF][START_REF] Gandevia | Does the nervous system depend on kinesthetic information to control natural limb movements[END_REF]Goble & Brown, 2008b;[START_REF] Pearson | Proprioceptive Sensory Feedback[END_REF][START_REF] Proske | The proprioceptive senses: Their roles in signaling body shape, body position and movement, and muscle force[END_REF][START_REF] Tuthill | Proprioception[END_REF]. These multiple receptors, distributed throughout the body, provide input to the central nervous system such that we perceive the state of our body parts and control over their movements [START_REF] Gardner | The somatosensory system: receptors and central pathways[END_REF][START_REF] Hall | Detections of movements imposed on finger, elbow and shoulder joints[END_REF][START_REF] Lephart | Proprioception and neuromuscular control in joint stability[END_REF][START_REF] Tuthill | Proprioception[END_REF]. The role of proprioception in motor control has been well documented, notably for postural stability, motor coordination, and fine motor skills [START_REF] Gandevia | Does the nervous system depend on kinesthetic information to control natural limb movements[END_REF][START_REF] Pearson | Proprioceptive Sensory Feedback[END_REF][START_REF] Scott | A Functional Taxonomy of Bottom-Up Sensory Feedback Processing for Motor Actions[END_REF]. The role of proprioception with and without visual feedback has been well-illustrated by the consequences of proprioceptive loss on motor functions [START_REF] Jayasinghe | Somatosensory deafferentation reveals lateralized roles of proprioception in feedback and adaptive feedforward control of movement and posture[END_REF][START_REF] Rothwell | Manual motor performance in a deafferented man[END_REF][START_REF] Sarlegna | Internally driven control of reaching movements: A study on a proprioceptively deafferented subject[END_REF][START_REF] Sarlegna | Forcefield adaptation without proprioception: Can vision be used to model limb dynamics?[END_REF]. Considering the critical role of proprioception in the perception and control of postures and movements and considering the body's widespread proprioceptors, a key question is "Is proprioception uniform across the body?" Several researchers have used varied methodologies to address this question by examining whether proprioception differs across upper limbs and joints. For instance, previous research investigated how proprioception at the elbow compares with that at the wrist, and better proprioceptive acuity has been found at the elbow using a movement detection threshold task [START_REF] Sturnieks | Detection of simultaneous movement at two human arm joints[END_REF] and active matching tasks [START_REF] Li | Clinical evaluation of motion and position sense in the upper extremities of the elderly using motion analysis system[END_REF][START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF]. Specifically, [START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF] had an experimenter moving blindfolded participants' joints for them to a specific reference angle. Participants were instructed to memorize this reference angle before their joint was passively moved back to a starting position. Participants had to match their memorized reference angle with active movement of the same limb. [START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF] showed that active matching errors were less variable at the elbow than at the wrist, though [START_REF] Tripp | A comparison of individual joint contributions to multijoint position reproduction acuity in overhead-throwing athletes[END_REF], in an earlier study, had not detected significant differences in participants' errors between the wrist and elbow in a multi-joint, threedimensional active matching task.

In this type of active matching task, the tested joint is actively or passively rotated to a specified reference angle, and the participant is asked to actively move the ipsilateral [START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF] or contralateral joint [START_REF] Li | Clinical evaluation of motion and position sense in the upper extremities of the elderly using motion analysis system[END_REF] to match that reference angle. An error is then quantified as the difference between the reference angle and the participant's actual matching angle. A limitation of active matching is that it precludes distinct assessments of the underlying proprioceptive perception processes and motor control processes. Indeed, motor commands can also be used to estimate position and motion states [START_REF] Desmurget | Forward modeling allows feedback control for fast reaching movements[END_REF][START_REF] Gandevia | Proprioception, tensegrity, and motor control[END_REF][START_REF] Gandevia | Motor commands contribute to human position sense[END_REF][START_REF] Smith | Signals of motor command bias joint position sense in the presence of feedback from proprioceptors[END_REF]. Because such central motor control signals may contribute differently to joint position sense at the elbow and wrist [START_REF] Walsh | The contribution of motor commands to position sense differs between elbow and wrist[END_REF], passive movement tasks appear to be most suited for assessing proprioceptive perception [START_REF] Carey | Impaired limb position sense after stroke: A quantitative test for clinical use[END_REF][START_REF] Goble | Upper limb asymmetries in the perception of proprioceptively determined dynamic position sense[END_REF][START_REF] Khabie | The effect of intraarticular anasthesia and elastic bandage on elbow proprioception[END_REF].

The uniformity of upper limb proprioceptive perception can be studied across joints but also across the preferred and the non-preferred limbs. Several investigators, utilizing ipsilateral active matching, reported a better joint position sense at the nonpreferred thumb [START_REF] Colley | Spatial Location Judgements by Right and Left-Handers[END_REF][START_REF] Roy | Handedness Effects in Kinesthetic Spatial Location Judgements[END_REF] and elbow [START_REF] Kurian | Left-arm dominance in active positioning[END_REF]. Similarly, others, utilizing a contralateral active matching task, reported a better joint position sense at the non-preferred elbow [START_REF] Goble | Upper limb asymmetries in the utilization of proprioceptive feedback[END_REF][START_REF] Goble | Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement[END_REF] and wrist [START_REF] Adamo | Position sense asymmetry[END_REF]. Also, at the elbow, Goble and Brown, (2010) used both ipsilateral and contralateral passive matching and showed better joint position sense of the non-preferred versus preferred limb. In contrast, others failed to find interlimb differences (a) at the shoulder, elbow, and wrist joints when using a contralateral active matching task [START_REF] Li | Clinical evaluation of motion and position sense in the upper extremities of the elderly using motion analysis system[END_REF][START_REF] Ramsay | Position-matching in the upper limb: Professional ballet dancers perform with outstanding accuracy[END_REF]; (b) at the shoulder and elbow when using an ipsilateral active matching task [START_REF] King | The shoulder and elbow joints and right and left sides demonstrate similar joint position sense[END_REF]; and (c) at the elbow [START_REF] Khabie | The effect of intraarticular anasthesia and elastic bandage on elbow proprioception[END_REF] and wrist [START_REF] Carey | Impaired limb position sense after stroke: A quantitative test for clinical use[END_REF] when using an ipsilateral passive matching task. This lack of consensus about upper limb proprioception might be related to the different research methodologies (ipsilateral/contralateral, active/passive).

One additional issue with contralateral matching is that sensory contributions (and motor contributions in active protocols) are required from both left and right body segments [START_REF] Allen | Effects of muscle conditioning on position sense at the human forearm during loading or fatigue of elbow flexors and the role of the sense of effort[END_REF][START_REF] Izumizaki | The illusion of changed position and movement from vibrating one arm is altered by vision or movement of the other arm[END_REF][START_REF] White | Illusions of forearm displacement during vibration of elbow muscles in humans[END_REF]. As the contributions from both the arms and the hemispheres of the brain are known to differ [START_REF] Goble | Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement[END_REF][START_REF] Sainburg | Convergent models of handedness and brain lateralization[END_REF], the interpretation of the results of studies using contralateral matching tasks is not straightforward.

Our main goal in the present study was to assess proprioceptive perception at the elbow and wrist of both upper limbs across consecutive responses and determine whether proprioceptive errors vary across joints and responses. We were also interested in determining whether participants with relatively good proprioceptive perception at a specific joint also had good perception at another joint. Previous research which investigated whether proprioceptive perception is a general ability (or, in other words, is similar all over the body) or is site-specific, found only significant correlations between right and left joints of both upper and lower limbs (finger, shoulder, ankle or knee) with no significant correlations found between ipsilateral joints such as the right shoulder and finger of the right hand [START_REF] Waddington | Ability to discriminate movements at the ankle and knee is joint specific[END_REF]Han et al., 2013a,b). The lack of significant correlation between data from different joints suggested that proprioception is not a global, general ability and would be better described as sitespecific.

Based on prior research, we hypothesized that proprioceptive perception would be better at the elbow compared to the wrist, and at the non-preferred versus preferred limb. We tested these hypotheses using an ipsilateral passive matching task.

Method

Participants

To determine the minimum sample size no required for this study, we performed a statistical power analysis using G*Power software (version 3.1.9.6; Kiel University, Kiel, Germany) and based our sample size calculation on the effect size of previous studies reporting proprioceptive differences between upper limbs [START_REF] Goble | Upper limb asymmetries in the perception of proprioceptively determined dynamic position sense[END_REF]; partial η 2 =0.29) and between joints [START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF]; partial η 2 =0.189).

To determine the minimum required sample size, we used the smallest partial η 2 (which corresponded to the smallest effect size) in [START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF]. For a F-test, repeated-measures, within factors 2x2x8 ANOVA (number of measurements=32) with a partial η 2 of 0.189 (corresponding to effect size of 0.48), the a priori power analysis indicated that for an alpha level of 0.05 and a power of 0.95, the minimum required sample size was estimated to be four. In the present study, we tested seven healthy adult participants (3 females, 4 males; Mage = 59.3, SD = 7.0 years; age range = 49-67 years).

None of the participants reported any neurological or musculoskeletal deficits.

Participants were recruited from the University and the city of Marseille through an advertisement email. All participants showed a strong right-hand preference, quantified with the 10-item version of the Edinburgh handedness inventory (Appendix A in Oldfield 1971). The participants' mean laterality quotient on this scale was 94.2% (SD = 9.7%). All participants gave their written informed consent before they participated, and no participants were compensated for their involvement. The experiment was approved by the national ethics committee CERSTAPS (IRB00012476-2020-03-06-60).

Experimental setup

Each participant was seated in an adjustable chair with each hand grasping a handle and both forearms lightly wrapped with fabric fasteners (Velcro) to the moving levers of the apparatus (as in [START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF]. The setup was precisely adjusted for each participant to align its mechanical rotation axes with the elbow and wrist rotation axes.

It allowed near-frictionless movement of the wrist in the sagittal plane and the elbow in the horizontal plane.

Joint rotations were recorded with precision potentiometers (linear, 10 kΩ, Vishay) mounted beneath the pivot point of the corresponding lever arms. Each potentiometer was connected to an analog-to-digital converter, and signals were sampled at 10 Hz. Data were recorded using a LabView Virtual Instrument (National Instruments Corporation, Austin, TX, USA).

During the task, all participants were blindfolded, and the experimenter moved one of the participant's upper limb body segments. The experimenter avoided reaching extreme ranges of motion and used visual feedback on a computer screen to control movement speed below 5°/second, a threshold that corresponds to the speed above which passive movement detection plateaus [START_REF] Laprevotte | Movement detection thresholds reveal proprioceptive impairments in developmental dyslexia[END_REF].

Experimental procedure and conditions

Two experimenters presented the apparatus to the participants. While one joint was being tested, the others were locked. Figure 1 illustrates the ipsilateral passive matching task. For each of the seven participants, a session corresponded to eight responses collected for each of the four experimental conditions. Each session was composed as following: as in [START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF], one experimenter moved the body segment corresponding to the tested joint (forearm for elbow and hand for wrist) from a randomly varied starting position toward the reference angle. The reference angles were 20° of flexion for the elbow with respect to the full extension of the participant's arm in the device, and 20° of flexion for the wrist with respect to its neutral position. Once the reference angle was reached, the experimenter stabilized the joint at that angle as the participant was instructed to memorize the reference joint angle and to verbally indicate when they were ready to proceed. Participants were given the time deemed necessary to memorize the reference angle (typical time: 2 -8 seconds), and the experimenter then moved the participant's body segment cyclically around the reference angle over the same range (by approximately ±20° for the elbow and ±25° for the wrist) and over approximately the same speed (below 5°/second) for each participant. During the cyclic movement, participants were instructed to say 'top' each time they estimated that the joint angle corresponded to the memorized reference angle. On each 'top' signal, the second experimenter recorded the signalled angle value by clicking on a mouse while the experimenter continued the passive cyclic movement without interruption until eight responses were recorded, which marked the end of the session. In no case were participants given knowledge regarding their performance, as in [START_REF] Goble | Upper limb asymmetries in the perception of proprioceptively determined dynamic position sense[END_REF]. The first session corresponded to the right wrist, the second to the right elbow, the third to the left wrist, and the fourth to the left elbow. In order to be able to compare individual differences, we fixed the order of the sessions, as illustrated in Figure 2.

However, to assess whether performance varied along the whole experiment and to assess test-retest reliability, we used a fifth session consisting of repeating the first session (performed with the right wrist) at the end of the experiment. Participants were given a short break between sessions, but they were not given any feedback about their performance during the experiment.

Data analysis

We computed four types of participant errors (in degrees) as had been done in previous research (Goble & Brown, 2008b;[START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF]Forestier et al., 2002) to characterize the accuracy and consistency of the matching performance:

• The signed error was calculated as the angular difference between the reported joint angle and the true reference angle (as in [START_REF] Goble | Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement[END_REF] and was used to determine the existence of any directional bias in matching accuracy.

Positive signed errors were assigned to more flexed joint angles compared to the reference, and negative signed errors were assigned to more extended joint angles.

• The variable signed error was calculated as the standard deviation around the mean of each participant's eight signed errors. It was used to assess the consistency of the directional bias.

• The absolute error was calculated as the absolute difference between the reported joint angles and the reference angles (as in [START_REF] Goble | Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement[END_REF] and was used to determine the extent of matching accuracy. The absolute error allowed us to focus on the magnitude of errors, irrespective of their positive or negative direction.

• The variable absolute error [START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF] was calculated as the standard deviation around the mean of each participant's eight absolute errors. It was used to assess the consistency of the extent of matching accuracy.

Eight responses were recorded for each of the five sessions, resulting in a total of 40 responses for each participant and 280 responses for all participants. We used a 2x2x8 analysis of variance (ANOVA) with repeated measures to determine the main effects of joint (wrist, elbow), laterality (right, left), and response (1 to 8) as well as their interactions for both signed and absolute errors. We used 2x2 ANOVAs with repeated measures to determine the main effects of the Joint (wrist, elbow) and Laterality (right, left) as well as their interaction for both variable signed errors and variable absolute errors.

We used linear correlation analyses to determine the relationship of the participants' errors between the two wrists, the two elbows, and the wrist and elbow of each limb; and to determine the relationship of the participants' errors with their age.

Pearson correlation coefficients (r) were calculated and interpreted according to their sizes [strong (r=0.7-0.89), moderate (r=0.5-0.69), or weak (r=0.1-0.39), as in Schober and Schwarte ( 2018)].

We assessed within-day test-retest reliability, or in other words, the potential effect of test variability (due to repetition, fatigue, change of mood, etc.) when comparing data from the first and last session. We analysed the correlation of these data and calculated the Pearson correlation coefficient (r). In addition, we used a 2x8 ANOVA with repeated measures to determine the main effects of Test (first test, last test) and Response (1 to 8) as well as their interaction on mean errors. We used a paired t-test to determine the effect of Test on variable errors.

All data presented a normal distribution as verified with the Kolmogorov-Smirnov method. Statistical significance was set at p<0.05. Post hoc comparisons were performed based on Tukey's honestly significant difference method [START_REF] Adamo | Position sense asymmetry[END_REF][START_REF] Goble | Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement[END_REF]. All ANOVA analyses and all post hoc comparisons were pre-planned. Data are available upon reasonable request.

Results

Signed error: differences between joints and responses.

Calculating the signed error allowed us to assess the direction of the error, with positive errors corresponding to perceiving the joint as more flexed than the reference angle.

Figure 3 shows that signed error varied as a function of the joint and the response number. A 2x2x8 ANOVA [Joint (elbow, wrist) x Laterality (left, right) x Response (1 to 8)] revealed a significant joint effect (F(1,6)=14.9, p=0.008, partial η 2 =0.713) on the signed error, which differed at the wrist (M = -4.7, SD = 2.5°) compared to the elbow (M = 4.2, SD = 4.6°). However, one cannot conclude from this analysis whether proprioceptive perception is more accurate for one joint or the other, as error magnitude was ~4.5° in both conditions. This ANOVA also revealed a significant response effect (F(7,42)=5.3, p<0.001, partial η 2 =0.473). Tukey's post-hoc analysis showed that the signed error in the first response significantly differed from the second, fourth, sixth, and eighth responses, and the signed error in the sixth response also differed from that in the third response.

There was a significant joint and response interaction effect (F(7,42)=6.3, p<0.001, partial η 2 =0.511) as shown in Figure 3, with a response effect on signed error only at the wrist and not at the elbow. An oscillatory pattern and a shift from positive to negative errors can be seen on wrist data, but the main statistical finding from post-hoc tests was that the first response differed from most other responses. Indeed, Tukey's post-hoc analysis showed that at the wrist, the signed error of the first response significantly differed from almost all the subsequent responses (i.e., responses 2, 4, 6, 7, and 8). From the second response to the last one, participants responded when their wrist was slightly less flexed than the reference angle. The second response differed from the third and the fifth. The third differed from the fourth, sixth and eighth. The fourth differed from the fifth and the fifth differed from the sixth and eighth. In contrast, at the elbow, there was no significant difference between responses which were consistently biased toward a slight flexion compared to the reference angle. There was no significant laterality effect (F(1,6)=1.1, p=0.34, partial η 2 =0.152), and there were no other significant interactions [Laterality x Joint (F(1,6)=0.01, p=0.91, partial η 2 =0.002), Laterality x Response (F(7,42)=0.3, p=0.96, partial η 2 =0.041), double interaction (F(7,42)=0.7, p=0.70, partial η 2 = 0.101)]. Variable signed error: differences between upper-limbs and joints A 2x2 ANOVA on the variable signed error revealed a significant joint effect (F(1,6)=34.6, p=0.001, partial η 2 =0.853), as the variable signed error at the elbow (M =5.1. SD = 1.7°) was significantly smaller than at the wrist (M = 7.9, SD = 1.9°). A significant laterality effect (F(1,6)=17.4, p=0.006, partial η 2 =0.743) was associated with a smaller variable signed error at the left arm (M = 5.7, SD = 1.5°) compared to the right (M = 7.3, SD = 1.9°). There was also a significant interaction effect of laterality and joint (F(1,6)=10.3, p=0.018, partial η 2 =0.633), illustrated in Figure 4, showing that the variable signed error was smaller at the left elbow (M = 3.7 , SD = 1.4°) compared to the right elbow (M =6.4, SD = 2.1°, p=0.008), the left wrist (M =7.8, SD= 2.0 °, p =0.001) and the right wrist (M = 8.1, SD= 1.8°, p<0.001). There were no significant differences between the variable signed error at the left and right wrists (p=0.94), the right elbow and the right wrist (p=0.08), and the right elbow and the left wrist (p=0.17).

In summary for this analysis, the smallest variable signed error was found at the left elbow compared to the right elbow and both wrists.

A 2x2x8 ANOVA on mean absolute error revealed only a significant interaction effect of joint and response (F(7,42)=4.2, p=0.001, partial η 2 =0.409), but post-hoc analysis showed no significant pairwise differences. Overall, there were no significant main effects for laterality (F(1,6)=1.2, p=0.32, partial η 2 =0.163), joint (F(1,6)=3.1, p=0.12, partial η 2 =0.342), and response (F(7,42)=0.5, p=0.81, partial η 2 =0.081) and no other significant interactions for laterality and joint (F(1,6)=0.5, p=0.50, partial η 2 =0.080), laterality and response (F(7,42)=0.5, p=0.86, partial η 2 =0.071), or double interaction (F(7,42)=0.4,p=0.88, partial η 2 =0.067). Overall, participants' absolute error averaged 5.6 (SD = 2.7°) at the left elbow, 6.8 (SD = 3.3°) at the right elbow, 7.7 (SD = 1.6°) at the left wrist and 7.9 (SD = 2.5°) at the right wrist.

Variable absolute error: differences between limbs and joints

Consistent with the statistical analysis of the variable signed error, a 2x2 ANOVA on the variable absolute error revealed significant main effects of joint (F(1,6)=7.4, p=0.03, partial η 2 =0.554) and laterality (F(1,6)=11.8, p=0.01, partial η 2 =0.663). Figure 5 shows that the variable absolute error at the elbow (M = 4.1, SD = 1.7°) was smaller than at the wrist (M = 5.3, SD = 1.2°). Also, the variable absolute error at the left limb (M = 4.0, SD = 0.9°) was smaller than at the right limb (M =5.3, SD = 1.8°). Group means and individual data are reported in Figure 5 to highlight the systematic nature of the results.

There was no significant interaction effect for laterality and joint (F(1,6)=1.7, p=0.24, partial η 2 =0.220). In summary, the variable absolute error was smaller at the elbow compared to the wrist, and at the left limb compared to the right limb.

Correlations between errors across participants

Correlations were used to determine whether participants with smaller or greater errors for a specific condition tended to have smaller or greater errors for another condition.

For the signed error, we found a strong linear, positive correlation between errors at the left and right elbows across participants (right elbow = 0.8 x left elbow + 1. 3, r=0.79, p=0.03). This is shown in Figure 6 For the absolute error, no significant linear correlations were found [left wrist and left elbow (r=-0.08, p=0.86), right wrist and right elbow (r=0.57, p=0.18), left and right wrists (r=0.41, p=0.36), left and right elbows (r=0.58, p=0.17)]. For the variable absolute error, no significant linear correlations were found [left wrist and left elbow (r=0.33, p=0.47), right wrist and right elbow (r=0.42, p=0.35), left and right wrists (r=0.48, p=0.28), left and right elbows (r=0.63, p=0.13)]. For the absolute errors as well as all other errors, there were no significant correlations with participants' ages (all P > 0.35).

Test-retest reliability

The right wrist was tested at the beginning and at the end of the experiment. Strong significant correlations were found between the first and the last tests for the signed error (right wrist last = 0.8 x right wrist first + 0.5, r=0.80, p=0.03) and the absolute error (right wrist last = 1.2 x right wrist first -1.8, r=0.85, p=0.01), as shown in Figure 8. No other significant correlations were found for the variable signed error (r=0.37, p=0.4) nor the variable absolute error (r=0.01, p=0.8). A 2x8 ANOVA [Test (First, Last) x Response (1 to 8)] on the signed error revealed no significant main test effect (F(1,6)=3.7, p=0.10, partial η 2 =0.383).

However, there was a significant response effect (F(7,42)=3.5, p=0.005, partial η 2 =0.365) and a significant interaction effect of test and response (F(7,42)=2.4, p=0.04, partial η 2 =0.287), as shown in Figure 9. While for the first test, some responses significantly differed from others (response 1 differed from response 2, 4 6, and 8; and response 3 significantly differed from response 6), no significant differences were found between responses for the last test.

For the absolute error, there was no significant main effect of test (F(1,6)=0.3, p=0.63, partial η 2 =0.042), nor response (F(7,42)=0.8, p=0.63, partial η 2 =0.117), nor was there a significant interaction (F(7,42)=1.9, p=0.08, partial η 2 =0.247). Also, paired ttests revealed no significant test effect for the variable signed error (t(6)=0.2, p=0.86;

Cohen's d= 0.07) and the variable absolute error (t(6)=1.0, p=0.38; Cohen's d=0.36).

Discussion

This study sought to test the hypotheses that upper limb proprioception assessed through a passive matching task would be better at the elbow than at the wrist and at the non-preferred versus preferred arm. In general, our findings are consistent with both hypotheses (at least in this small sample of right-handers). We found that proprioception was more precise at the elbow than at the wrist as revealed by the small variable errors at the elbow. This was associated with better stability of the responses at the elbow. We also found that proprioception at the left limb was less variable than at the right limb.

We now further discuss these findings in greater detail.

Proprioceptive perception is more precise at the elbow compared to the wrist Proprioception at the elbow was less variable than at the wrist, and this was especially clear for the non-preferred arm, for both signed and absolute errors. This finding concurs with findings from [START_REF] Li | Clinical evaluation of motion and position sense in the upper extremities of the elderly using motion analysis system[END_REF], and [START_REF] Sevrez | On the Role of Proprioception in Making Free Throws in Basketball[END_REF] whose studies showed that perceiving unseen passive positions and motions at the elbow joint was more accurate than at the wrist. Similarly, [START_REF] Hall | Detections of movements imposed on finger, elbow and shoulder joints[END_REF] found that proprioceptive acuity was higher at upper limb joints more proximal to the brain (shoulder and elbow) than a more peripheral joint (middle finger's most distal joint).

The better proprioceptive perception at proximal joints may reflect the important role these joints play in determining the location of the endpoint [START_REF] Scott | The computation of position sense from spindles in mono-and multiarticular muscles[END_REF].

Proprioceptive differences between the elbow and wrist joints may also be associated with the larger spindle counts found at the muscles crossing the elbow compared to those crossing the wrist [START_REF] Scott | The computation of position sense from spindles in mono-and multiarticular muscles[END_REF]. Muscle spindles are known to provide most of the afferent information for proprioception [START_REF] Gandevia | Does the nervous system depend on kinesthetic information to control natural limb movements[END_REF][START_REF] Tuthill | Proprioception[END_REF]) by detecting the change in fascicle length per degree of joint rotation with great sensitivity [START_REF] Hall | Detections of movements imposed on finger, elbow and shoulder joints[END_REF]. The distribution of spindles among and within individual muscles is highly specific and constant among individuals [START_REF] Banks | Quantitative Studies on Mammalian Muscle Spindles and their Sensory Innervation[END_REF][START_REF] Matthews | Mammalian Muscle Receptors and Central Actions[END_REF][START_REF] Matthews | Proprioceptors and their contribution to somatosensory mapping: Complex messages require complex processing[END_REF]. The heterogeneous distribution of spindles would appear to benefit the elbow over the wrist.

It is possible that the reference angle and movement plane differentially influenced proprioceptive perception at the elbow, compared to the wrist. [START_REF] Goble | Upper limb asymmetries in the perception of proprioceptively determined dynamic position sense[END_REF] previously showed that larger reference angles induced larger proprioceptive errors at the elbow, although [START_REF] Marini | The effects of age and amplitude on wrist proprioceptive acuity[END_REF] failed to find an angle effect on the wrist in flexion-extension degree of freedom. The reference angle for the elbow was approximately in the middle of the elbow's range of motion, while the reference angle for the wrist corresponded approximately to the third of the wrist's range of motion (from a fully flexed position). Moreover, the elbow was moved in the horizontal plane while the wrist was moved in the vertical plane. While [START_REF] Sturnieks | Detection of simultaneous movement at two human arm joints[END_REF] found no significant difference in detection thresholds for wrist movements in the two planes, [START_REF] Darling | Kinesthetic perceptions of earth-and body-fixed axes[END_REF] suggested that the gravitational vertical axis could be one of the preferred axes for proprioceptive perception. Therefore, movement plane, and/or gravity, may have influenced matching errors in the present study. Further research is needed to compare proprioceptive perception between joints in the same movement plane and using the same reference angle with respect to the range of motion.

Proprioceptive perception is more precise at the non-preferred upper limb

Our study provided additional evidence of a proprioceptive advantage at the nonpreferred upper limb. Indeed, our results showed that proprioceptive variability was smaller for the non-preferred arm, particularly for the non-preferred elbow. These results confirm and extend previous results, supporting the view of lateralization of proprioceptive function. More specifically, our findings are consistent with previous studies showing a non-preferred limb advantage at the thumb [START_REF] Colley | Spatial Location Judgements by Right and Left-Handers[END_REF][START_REF] Roy | Handedness Effects in Kinesthetic Spatial Location Judgements[END_REF] and elbow [START_REF] Goble | Upper limb asymmetries in the perception of proprioceptively determined dynamic position sense[END_REF][START_REF] Kurian | Left-arm dominance in active positioning[END_REF] using active/passive matching tasks; and at the shoulders and fingers using an active movement extent discrimination task [START_REF] Han | Proprioceptive performance of bilateral upper and lower limb joints : side-general and site-specific effects[END_REF]. [START_REF] Han | Proprioceptive performance of bilateral upper and lower limb joints : side-general and site-specific effects[END_REF] found that for multiple joints (fingers, shoulders, ankles and knees), proprioceptive performance on the non-preferred left limb was significantly better than the preferred right limb. A laterality effect was thus found with both an active method [START_REF] Han | Proprioceptive performance of bilateral upper and lower limb joints : side-general and site-specific effects[END_REF]) and a passive method in the present study; and overall, findings support the view of a non-preferred limb advantage in proprioception.

Even though we obtained evidence that proprioceptive perception is lateralized, we found strong, positive correlations between signed errors at the preferred and nonpreferred elbows. We also found strong, positive correlations between variable signed errors at the preferred and non-preferred wrists. These findings support previous research which reported, using an active movement extent discrimination task, significant correlations between left and right joints at the upper limbs (finger and shoulder; [START_REF] Han | Proprioceptive performance of bilateral upper and lower limb joints : side-general and site-specific effects[END_REF] and significant correlations between left and right joints at the lower limbs (ankle and knee; [START_REF] Waddington | Ability to discriminate movements at the ankle and knee is joint specific[END_REF], but not between ipsilateral joints. Altogether, these results suggest that proprioceptive errors may be smaller for the non-preferred upper limb compared to the preferred upper-limb but also that proprioceptive errors may be correlated between right and left upper limbs. It thus would appear that an individual with relatively small proprioceptive errors at one joint also has relatively small proprioceptive errors at the contralateral joint. This lateralization of proprioception may, to a certain extent, be associated with the functional roles of each upper limb. The postural and motor control of the nonpreferred arm may rely more on proprioceptive information than the preferred arm [START_REF] Sainburg | Convergent models of handedness and brain lateralization[END_REF]. Goble and Brown (2008a) found a proprioceptive advantage at the nonpreferred arm in the proprioceptive condition during an active elbow matching task. They reported that both mean absolute errors and variable absolute errors were smaller for the non-preferred elbow. One working hypothesis is that the nonpreferred arm relies more on proprioceptive information compared to the preferred arm which can be controlled based on efficient feedforward and visual feedback mechanisms for several tasks. Another possible explanation for the asymmetric proprioceptive perception found here and elsewhere in the literature is a hemispheric lateralization of proprioceptive processing. The better proprioceptive perception for the non-preferred arm of right-handers would be associated with a right hemisphere specialization for processing proprioceptive signals, a hypothesis that has been further supported by neuroimaging studies. For instance, [START_REF] Naito | Dominance of the right hemisphere and role of area 2 in human kinesthesia[END_REF][START_REF] Naito | Human limb-specific and non-limb-specific brain representations during kinesthetic illusory movements of the upper and lower extremities[END_REF] investigated brain regions responsible for processing signals from muscle spindle proprioceptors using tendon vibration and these researchers provided evidence for right hemisphere dominance for processing proprioceptive signals. This hemispheric specialization would suggest that individuals with right-hemisphere damage would be more prone to proprioceptive deficits. This was reported by [START_REF] Goble | Deficits in the ability to use proprioceptive feedback in children with hemiplegic cerebral palsy[END_REF] who tested children with hemiplegic cerebral palsy in an ipsilateral elbow active matching task (see also Leonard & Milner, 1995).

Our results of interlimb differences in proprioceptive perception contrast with those of other studies that found no significant laterality effect when using ipsilateral active matching tasks at the elbow [START_REF] Goble | Upper limb asymmetries in the utilization of proprioceptive feedback[END_REF][START_REF] Goble | Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement[END_REF] and wrist [START_REF] Adamo | Position sense asymmetry[END_REF] of right-handed participants, or when using an ipsilateral passive matching task at the wrist [START_REF] Carey | Impaired limb position sense after stroke: A quantitative test for clinical use[END_REF] and elbow [START_REF] Khabie | The effect of intraarticular anasthesia and elastic bandage on elbow proprioception[END_REF].

However, these studies did not assess variable errors that are considered important to characterize proprioceptive performance. Also, some of these studies reported a better accuracy of the non-preferred limb during contralateral active matching tasks [START_REF] Adamo | Position sense asymmetry[END_REF][START_REF] Goble | Upper limb asymmetries in the utilization of proprioceptive feedback[END_REF][START_REF] Goble | Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement[END_REF]. Moreover, [START_REF] Goble | Upper limb asymmetries in the perception of proprioceptively determined dynamic position sense[END_REF] reported better proprioceptive perception at the non-preferred elbow in a passive detection task. While elbow proprioception does appear to be better at the non-preferred limb, further research with active and passive and with contralateral and ipsilateral matching is necessary to clarify the issue of lateralization of proprioceptive perception.

Limitations and Directions for Further Study

This study has some limitations requiring our findings to be interpreted carefully. Our participant sample size was limited to seven. Although this number is sufficient for detecting statistically significant differences, increasing the sample size and further varying participant ages would allow more generalizability of these findings. Also, we did not control potentially confounding factors such as participants' working memory, their sport and physical activity (see for instance [START_REF] Goble | Compromised encoding of proprioceptively determined joint angles in older adults: The role of working memory and attentional load[END_REF][START_REF] Ribeiro | Aging effects on joint proprioception: The role of physical activity in proprioception preservation[END_REF][START_REF] Ribeiro | Aging effects on joint proprioception: The role of physical activity in proprioception preservation[END_REF], and muscle thixotropy. Muscle thixotropy describes the fact that resistance of muscles is temporarily reduced during movement, whether due to externally applied or internally generated forces. Even though our data were collected during a continuous movement, it is possible that muscle thixotropy, during the static state of reference memorization, influenced the ensuing responses, as muscle thixotropy is maximum in stationary conditions and is known to influence proprioception [START_REF] Proske | Muscle thixotropy as a tool in the study of proprioception[END_REF][START_REF] Lakie | Muscle thixotropywhere are we now[END_REF]. Future work should thus take into account muscle thixotropy to design protocols to evaluate proprioception. Finally, we used a continuous movement task that may have influenced the reported errors by introducing a response delay between the 'top' of the participant and the mouse click of the experimenter. Even though we did our best to minimize the potential influence of the delay on our measures by using a low movement speed and the same experimenter in all conditions, further work should rely on direct, automated measures.

Conclusion

Overall, proprioceptive perception appears to be more consistent at the non-preferred arm compared to the preferred arm, and more consistent at the elbow compared to the wrist. Our findings thus suggest that the precision of proprioception, as reflected by the variability of our measures, differs across joints and limbs. The joint specificity and lateralization of proprioceptive measures suggest that assessing proprioception at a single joint is not representative of a general assessment of an individual's proprioception. Multiple joint testing may be necessary to screen for possible 40 proprioceptive deficits. Our findings may also be considered when designing rehabilitation protocols, as it remains unclear whether proprioceptive training at one joint will generalize to another joint, on the same or opposite limb. To conclude, the present study suggests that signed errors and variable signed errors may be the most discriminative measures when assessing the influence of laterality and joint differences on upper limb proprioception. Our findings thus highlight the importance of analysing variable errors when assessing proprioceptive perception.

186 187Figure 1 :

 1861 Figure 1: Illustration of the Ipsilateral Passive Matching Task. A. Side view of the participant. B. Top view of the participant. First (left panel), the tested joint was passively moved toward the reference angle (between the orange line and the dashed line) for memorization. Then (middle panel), it was passively and continuously moved around the reference angle. During this passive movement, participants were requested to verbally indicate (right panel) each time they detected that the current angle matched the reference angle. A session consisted of eight responses.

Figure 2 :

 2 Figure 2: Order of the Experimental Sessions.

Figure 3 :

 3 Figure 3: Mean Signed Error at the Wrist (filled squares), and Elbow (empty circles), for Each Response. Error bars represent standard deviation around the participants' mean.

Figure 4 :

 4 Figure 4: Variable Signed Error at the Wrist (filled squares), and Elbow (empty circles), for Each Response. Error bars represent standard deviation around the participants' mean.

Figure 5 :

 5 Figure 5: Variable Absolute Error for each Participant (colored dots) and Group Means (empty rectangles). Error bars represent the standard deviation around the participant's mean. (A) Joint effect. (B) Laterality effect.

  in which, for instance, one participant (blue dot) had the largest signed error at the right elbow and at the left elbow. No other significant correlations were found between errors at the left and right wrists (r=-0.03, p=0.94), left wrist and left elbow (r=-0.72, p=0.07), nor right wrist and right elbow (r=-0.33, p=0.47).

Figure 6 :Figure 7 :

 67 Figure 6: Relationship Between Mean Signed Errors at the Left and Right Elbows,for Each Participant (according to the same color code as in Figure5). The linear regression (dashed line) is displayed to aid visualization.

Figure 8 :

 8 Figure 8: Relationship Between Errors in the First and Last Tests for the Right Wrist of Each Participant (according to the same color code as in Figures 5-7). Each linear regression (dashed line) is displayed to aid visualization. (A) Mean signed error of each participant. (B) Mean absolute error of each participant.

Figure 9 :

 9 Figure 9: Right Wrist's Signed Errors for Each Response of the First (filled squares) and the Last (empty squares) Test Performed During the Experiment. Error bars represent the standard deviation around the participants' mean.

https://doi.org/10.1007/s00221-008-1561-z

Acknowledgments:

We would like to thank the subjects for participating in the study;

Rochelle Ackerley for helpful feedback on the manuscript; P. Sainton for technical assistance.

Conflict of interest.

Authors report no conflict of interest.