Lower Limb Proprioception and Strength Differences Between Adolescents With Autism Spectrum Disorder and Neurotypical Controls

Abstract

Autism spectrum disorder (ASD) is a complex diagnosis characterized primarily by persistent deficits in social communication/interaction and repetitive behavior patterns, interests, and/or activities. ASD is also characterized by various physiological and/or behavioral features that span sensory, neurological, and neuromotor function. Although problems with lower body coordination and control have been noted, little prior research has examined lower extremity strength and proprioception, a process requiring integration of sensorimotor information to locate body/limbs in space. We designed this study to compare lower limb proprioception and strength in adolescents with ASD and neurotypical controls. Adolescents diagnosed with ASD (n = 17) and matched controls (n = 17) performed ankle plantarflexion/dorsiflexion bilateral proprioception and strength tests on an isokinetic dynamometer. We assessed position-based proprioception using three targeted positions (5 and 20-degrees plantarflexion and 10-degrees dorsiflexion) and speed-based proprioception using two targeted speeds (60 and 120-degrees/second). We assessed strength at 60-degrees/second. Participants with ASD performed 1.3-times more poorly during plantarflexion position and 2-times more poorly during the speed-based proprioception tests compared to controls. Participants with ASD also exhibited a 40% reduction in plantarflexion strength compared to controls. These findings provide insight into mechanisms that underly the reduced coordination, aberrant gait mechanics, and coordination problems often seen in individuals with ASD, and the identification of these mechanisms now permits better targeting of rehabilitative goals in treatment programs.

Keywords

autism spectrum disorder proprioception sensorimotor feedback exercise lower extremity

Introduction

Autism spectrum disorder (ASD) is a neurodevelopmental disorder estimated to affect 1 in 59 children in the US (Zablotsky et al., 2015). ASD is a complex diagnosis characterized primarily by social communication/interaction problems and repetitive behavior patterns, interests, or activities but also by various physiological and/or behavioral features that span sensory, neurological, and neuromotor function (American Psychiatric Association, 2013). Significant evidence also indicates a prevalence of motor deficits among those with ASD (Fournier et al., 2010), including problems with postural control, gait, coordination, and both gross and fine motor skills (Armitano et al., 2020; Bennett et al., 2021; Blank et al., 2019; Calhoun et al., 2011; Fournier et al., 2010; Kern et al., 2013; Morris et al., 2015; Morrison et al., 2018).

The ability to perform everyday tasks (e.g., maintain postural control and execute and coordinate goal-directed movements) is vital for the development of social interactions, communication skills, and play skills (Clearfield, 2011; MacDonald et al., 2013). Consequently, these known motor skill deficits have been proposed to contribute significantly to the social impairments that typify individuals with ASD (Bhat et al., 2011). Indeed, Blank et al. (2019) has noted that Developmental Coordination Disorder (DCD), an under-studied concern, is often associated with ASD and other neurodevelopmental disorders (Blank et al., 2019). While descriptions of motor differences are found in the earliest descriptions of ASD, researchers have only recently begun to better understand and specify the underlying motor deficits in ASD (e.g., (Blank et al., 2019; Cacola et al., 2017)) that may assist its early detection and remediation. For instance, muscle weakness is believed to be one of the earliest ASD motor signs (Bhat et al., 2011). When compared to neurotypical controls, individuals with ASD tend to exhibit reduced strength in the upper extremity (Lourenço et al., 2015), hand grip (Kern et al., 2011; 2013), and pinch grip (Alaniz et al., 2015). Further, research by Kern and colleagues revealed a strong relationship between grip strength and ASD severity (Kern et al., 2011). Interestingly, there is a limited amount of research evaluating lower extremity strength in this population, despite the influence of muscle weakness on balance, postural control, and coordination (Goldberg & Neptune, 2007; Horlings et al., 2008). To continue to advance our assessments and treatments of ASD and, specifically, to improve movement-related impairments in ASD, more research is needed to evaluate lower extremity strength differences between individuals with ASD and neurotypical controls.

Persons with ASD can also exhibit an impaired ability to regulate and organize sensory information (Ben-Sasson et al., 2009; Tomchek & Dunn, 2007) with a resulting significant impact on motor adaptability (Lane, 2002). The ability to integrate sensory information and produce an appropriate neuromuscular response permits task performance from upright standing (postural control) to walking (Hausdorff et al., 1999). Specifically, visual, vestibular, and proprioceptive feedback provide the brain with information necessary for adaptive and corrective muscular responses in order to maintain movement control (e.g., from postural control to gait) (Johansson & Magnusson, 1991; Maurer et al., 2006; Varraine et al., 2002). Sensory deficits in these areas could significantly impact motor performance.

The capacity to sense and locate joint and/or limb position and movement is integral to motor control; this process is known as proprioception. Somatosensory information derived from proprioceptors conveys this essential sensory information about the position and movement of a given joint and/or limb segment (Kavounoudias et al., 1999). Despite this critical role of proprioceptive information in everyday tasks, there has been little prior research that has explicitly examined proprioception in individuals with ASD. Extant research has focused predominantly on the influence of proprioception on postural control and balance (Minshew et al., 2004; Molloy et al., 2003; Morris et al., 2015; Travers et al., 2013) and on the performance of simple upper extremity motor tasks (Fuentes et al., 2011; Weimer et al., 2001). Surprisingly, however, no studies have investigated lower limb proprioceptive deficits in ASD, despite the importance of proprioceptive information on such specific motor skills as balance, coordination, and locomotion (Frost et al., 2015; Han et al., 2015; Rossignol et al., 2006; Sainburg et al., 1995) and previously discussed motor skill deficits associated with ASD.

We designed this study to fill this research gap by assessing and comparing lower limb proprioception in both adolescents with ASD and neurotypical adolescents. Our specific purpose was to examine ankle strength and level of proprioception capability in these two groups, matched regarding age, sex, and body mass index (BMI). Per previous research, we hypothesized that the ASD group would exhibit reduced strength and proprioceptive ability (i.e., greater error) compared to their matched controls.

Method

Participants

We recruited adolescents with ASD and neurotypical controls from the surrounding community using flyers, emails, and word of mouth. Participants with ASD were required to be between the ages of 13-18 years and to provide documentation confirming an ASD diagnosis. Diagnoses were based on both the DSM-IV and DSM-V diagnostic criteria. Participants were not required to present documentation of level of support. Neurotypical adolescents who were recruited for this study were matched according to age, sex, and BMI to a participant with ASD. Neurotypical adolescents had no clinical diagnosis of any social, physical, or sensory impairment. Along with participant demographics (e.g., age, mass, height), we determined the participants’ limb dominance by asking the participants and their guardians (for all participants aged less than 18 years) which leg the participant used to kick a ball. Exclusion criteria for all participants were any self-report or guardian report of current or recent (i.e., within six months) musculoskeletal injuries, joint disease, major joint surgery, joint replacement, or tested intelligence with an IQ standard score < 70. Participants were provided with video recordings of the exact procedures to be performed in this study to familiarize them with these procedures. We recruited a total of 34 participants who completed the study - 17 adolescents with ASD and 17 age, sex, and BMI-matched neurotypical controls (see Table 1).

Table 1.

Participant Characteristics in Means (and Standard Deviations).

Group	Age (yrs.)	Sex (M/F)	Mass (kg)	Height (m)	BMI
ASD	15.0 (1.5)	12/5	57.6 (18.4)	1.6 (0.1)	21.4 (5.4)
CON	14.5 (1.4)	12/5	59.6 (13.3)	1.7 (0.1)	20.4 (3.7)

Note. ASD: youth with autism spectrum disorder; CON: age, sex, and BMI- matched controls; yrs.: years; kg: kilograms; m: meters; BMI: body mass index. Matched controls were held within 1-year of age and within 2-BMI points of the corresponding youth with ASD.

Regarding the ethical treatment of our participants, this study was reviewed and approved by the Old Dominion University Institutional Review Board. Study procedures were reviewed with each participant and their legal guardian, where applicable. All participants and their legal guardians (for all participants aged less than 18 years), provided consent for participation in this study.

Testing Procedures

All participants completed strength, position-based proprioception, and speed-based proprioception tests using an isokinetic dynamometer. The strength test assessed strength of the surrounding ankle musculature at a constant speed. The position and speed-based proprioception test assessed participants’ proprioceptive capabilities to reproduce predefined angles and speeds, respectively. Performance on each test by the dominant limb and the average of both limbs were compared between the two groups.

Testing was performed on a HUMAC NORM Isokinetic Extremity System (CSMi, Inc.). Participants were instructed to lie prone on the dynamometer chair. The dynamometer arm and chair were adjusted such that the dynamometer arm joint coincided with the lateral malleolus of the tested limb. Then, we secured the foot plate attachment to the participant’s shoe and we determined the participant’s active ankle joint range of motion according to the manufacturer’s guidelines.

Each of the three tests were performed on each limb. Strength testing was performed at a predefined speed of 60°/sec. Position-based proprioception was performed at three predefined angles: 20° plantarflexion, 5° plantarflexion, and 10° dorsiflexion. The speed-based proprioception test was performed at two pre-defined speeds: 60°/sec and 120°/sec. The position and speed-based angles/speeds were chosen as they readily appear during walking. Range of motion during the strength and speed-based proprioception tests were limited to 20° plantarflexion and 10° dorsiflexion to ensure comfort and safety.

We randomized the order of testing of each limb (i.e., left/right) across all participants. Prior to beginning any test, participants were provided a familiarization period in which participants were instructed to move throughout their complete range of motion slowly, to push hard and soft against the foot plate, and to move fast and slow through whole and partial ranges of motion. The familiarization period was performed until the participant stated they felt comfortable with the setup. Participants were then asked to perform strength, position-based proprioception, and speed-based proprioception testing presented in a randomized order. We completed this protocol for a single limb and then repeated it for the contralateral limb. The protocol for both limbs generally required 30 minutes to complete.

Strength Testing

The strength protocol involved three sets of five repetitions of maximal effort contractions. Participants were instructed to “push and pull as hard and as fast as they can” to move the dynamometer arm. A warm-up/familiarization set was provided in which participants could complete as many (but at least five) repetitions as were necessary to feel comfortable with the testing procedures. A minimum of 60 seconds of rest were provided between sets, dependent upon the participant’s stated feelings of readiness. We recorded the maximum value for each repetition.

Position-Based Proprioception Testing

For the position-based proprioception test, the dynamometer moved the participant to the pre-defined position and locked the foot plate in position. The participant was then instructed to “Memorize where your foot is, how it is being held in place. Feel free to push and pull against the plate. When you think you have the position memorized, we will release the foot plate and begin the test.” After memorization, their foot was returned to the neutral position. Prior to testing, participants performed a familiarization protocol set at 10° plantarflexion. During familiarization, verbal feedback was given to the participant. For testing, the order of positions was randomized. The participant was instructed to repeat the position three times. The position for each repetition was recorded. No affirmative or negative feedback was provided during testing.

Speed-Based Proprioception Testing

For the speed-based proprioception test, the dynamometer demonstrated the test by moving the participants ankle through the range of motion at the pre-defined speed. Participants were instructed to memorize how fast their foot was moving. When the participant felt they could move at the same speed as the dynamometer, the demonstration was ended. Next, the participant was asked to move their foot through the range of motion, matching the previously demonstrated speed. Prior to testing, participants performed a familiarization protocol at 30°/sec. During familiarization, verbal feedback was given to the participant. Speeds at the midpoint of their range of motion were recorded for each repetition to reduce the inclusion of periods of acceleration (at beginning and end of movement). Due to the complexity of the task, and to represent “best efforts,” we used trials that most closely matched the pre-defined speeds for data analyses. The speed for each repetition was recorded. No affirmative or negative feedback was provided during testing.

Data Reduction and Statistical Analyses

Variables of interest for group comparisons were strength for the plantar and dorsiflexor muscle groups (normalized to body mass*height), absolute errors of the 5° plantarflexion, 10° dorsiflexion, and 20° plantarflexion position-based proprioception tests, and absolute errors of the 60°/sec and 120°/sec speed-based proprioception tests. Dominant and average limb data were both analyzed for each test to indicate uni- and/or bilateral deficits in those with ASD. Ensemble raw scores are also provided but were not compared statistically.

Data were imported into SPSS (version 26, IBM, inc.). All variables were checked for normality of data distributions using Shapiro-Wilks tests. Variables with normality concerns were transformed using logarithms (base 10). No variables required non-parametric testing due to persistent normality concerns. Group differences were determined using independent-samples t-tests. We implemented the Benjamini-Hochberg procedure with a false-discovery rate set at 0.10 to adjust significance levels for multiple-comparisons. Cohen’s D (d) effect size is reported for each variable and interpreted as small (d: 0.2 to 0.49), medium (d: 0.5 to 0.79), and large (d ≥ 0.8).

Results

Strength

Ensemble normalized strength data are shown in Table 2. Youth with ASD had decreased plantarflexor strength by 0.14 body mass*height (d = 2.21). No significant differences were found between groups for dorsiflexor strength (p > 0.05).

Table 2.

Mean (and Standard Deviation) Ankle Plantarflexor and Dorsiflexor Strength by Group.

Muscle group	Scheme	ASD	CON	Statistics (T, p, d)
Plantarflexor	Raw	21.4 (8.86)	38.2 (11.55)	N/A
Plantarflexor	Normalized	0.2 (0.06)	0.3 (0.06)	6.55, 5.43E-05, 2.21
Dorsiflexor	Raw	16.4 (5.53)	20.5 (5.14)	N/A
Dorsiflexor	Normalized	0.1 (0.04)	0.2 (0.04)	1.90, 0.071, 0.62

Note. ASD: youth with autism spectrum disorder; CON: age, sex, and BMI matched controls; Raw and normalized moments reported in Newton*meters and relative to body mass * height, respectively; T, p, d: T-statistic, p-value, and Cohen’s D effect size, respectively. Bolded statistics denote statistically significant differences between groups. No statistics were performed on raw strength data.

Position-Based Proprioception

Ensemble absolute errors for both position and speed-based proprioception tests are provided in Figures 1 and 2. Means per group and statistical test results for both position and speed-based proprioception tests are provided in Table 3. Youth with ASD performed more poorly on the 20-degree plantarflexion position test for the dominant limb by 2.8° (d = 0.74) and average of both limbs by 1.4° (d = 0.68; Table 3 and Figure 1(a)). No group differences were found for the 5° plantarflexion or 10° dorsiflexion tests (all p > 0.05; Table 3 and Figures 1 and 2).

Figure 1.

Ensemble Absolute Errors of all Proprioception Tasks for Dominant Limb (a) and the Average of Both Limbs (b). Average (columns) and one standard deviation (bars) absolute errors for the positional (P-20, P-5, D-10) and speed based (Sp-60 and Sp-120) tasks are reported in degrees and degrees/sec, respectively. P- and D- represent targeted plantarflexion and dorsiflexion angles. Stars denote statistically significant differences between youth with ASD (black) and matched controls (gray).

Figure 2.

Raw Scores for Position and Speed-Based Proprioception Tests of Dominant Limb (a) and the Average of Both Limbs (b). Youth with ASD (dark gray) and controls (light grey) average (columns) and one standard deviation (bars) raw scores for the positional (P-20, P-5, D-10) and speed based (Sp-60 and Sp-120) tasks are reported in degrees and degrees/sec, respectively. P- and D- represent targeted plantarflexion and dorsiflexion angles, where plantarflexion angles are positive and dorsiflexion angles are negative.

Table 3.

Mean (and Standard Deviation) Position and Velocity-based Proprioception Test Errors by Group.

Test	Limb	ASD	CON	Statistics (T, p, d)
P-20	Dominant	6.2 (4.3)	3.4 (2.9)	2.88, 0.005, 0.74
P-20	Average	5.6 (2.7)	4.2 (1.6)	2.06, 0.048, 0.68
P-5	Dominant	5.7 (4.6)	3.7 (2.1)	0.76, 0.462, 0.56
P-5	Average	5.1 (3.3)	3.9 (1.5)	1.45, 0.164, 0.48
D-10	Dominant	5.9 (4.6)	5.0 (3.6)	0.72, 0.483, 0.24
D-10	Average	5.0 (3.0)	5.0 (3.2)	0.38, 0.713, 0.02
Vel-60	Dominant	21.2 (15.7)	12.2 (11.6)	2.19, 0.032, 0.65
Vel-60	Average	24.4 (14.2)	10.1 (7.9)	3.69, 0.001, 1.24
Vel-120	Dominant	21.2 (15.7)	11.6 (8.1)	2.84, 0.005, 1.01
Vel-120	Average	30.9 (25.8)	12.8 (17.6)	2.40, 0.018, 0.88

Note. ASD: youth with autism spectrum disorder; CON: age, sex, and BMI matched controls; Position (P-20, P-5, P-10) and velocity (Vel-60 & Vel-120) test errors are reported in degrees and degrees/second, respectively, from their target (e.g. P-20 is 20 degrees of plantarflexion). T, p, d: T-statistic, p-value, and Cohen’s D effect size, respectively. Bolded statistics denote statistically significant differences between groups.

Speed-Based Proprioception

Youth with ASD performed more poorly on both speed-based tests for both the dominant limb and the average of both limbs (Table 3; Figures 1 and 2). Youth with ASD had 14.3°/sec (d = 1.24) and 15.7°/sec (d = 0.88) greater error in the dominant limb for the 60 and 120 speed tests, respectively. Youth with ASD also had 9.0°/sec (d = 0.65) and 19.3°/sec (d = 1.01) greater error for the average of both limb for the 60°/sec and 120°/sec speed tests, respectively.

Discussion

This study examined lower extremity strength along with position and speed-based proprioception in adolescents with ASD compared to age, sex, and BMI matched neurotypical controls. We hypothesized that youth with ASD would have reduced strength and increased error for both position and speed-based proprioception tests. Youth with ASD were characterized by reduced plantarflexion strength and reduced proprioceptive acuity, notably when assessing speed-based proprioception.

Our findings revealed moderate differences in proprioceptive position at the larger range of plantarflexion (i.e., 20 degrees) and large differences in both speed tests (Table 3). Specifically, participants with ASD performed nearly 1.3 times more poorly on plantarflexion position tests and two times more poorly on both speed-based tests than did their neurotypical counterparts (see Table 3). While this is the first study to specifically assess proprioception in the lower extremity, these findings are consistent with literature examining the influence of proprioception on postural control (Minshew et al., 2004; Molloy et al., 2003; Morris et al., 2015; Travers et al., 2013). Indeed, our results are of significance, especially since individuals with ASD have been reported rely more than others on proprioceptive over visual feedback in order to maintain postural control in the context of postural perturbations (Morris et al., 2015).

In addition to reduced lower limb proprioception, participants with ASD demonstrated significantly reduced plantarflexion strength compared to the control group. These results build upon the general premise that individuals with ASD demonstrate reduced strength compared to neurotypical controls (Kern et al., 2013; Morrison et al., 2018). Consequently, plantarflexion mobility and strength are necessary during normal gait to achieve a forceful push-off (Norris et al., 2007) in addition to playing a functional role in the control of forward movement during the swing phase of gait (Neptune et al., 2001). The markedly reduced ankle muscle strength in adolescents with ASD coincide with kinetic and kinematic evaluations of gait that have shown that those with ASD walk and run with decreased plantarflexion moments (Bennett & Haegele, 2021; Calhoun et al., 2011), plantarflexion angles (Ambrosini et al., 1998; Calhoun et al., 2011; Nobile et al., 2011), and range of motion across the lower extremity joints (ankle, knee, and hip; Nobile et al., 2011) compared to neurotypical controls. Reduced plantarflexion strength and diminished proprioception may impact the ability to adequately control more complex tasks involving the lower extremity, leading to the clumsy and less coordinated gait pattern characteristic of individuals with ASD.

Overall, the underestimation of target positional values by participants with ASD during the proprioception tasks and their reduced strength can be attributed to underlying neural mechanisms (Mosconi & Sweeney, 2015; Mostofsky et al., 2009). Resultant sensorimotor difficulties, such as poor coordination, reduced accuracy and an inability to perform complex motor tasks, are believed to contribute, in turn, to reduced physical activity on the part of individuals with ASD (Srinivasan et al., 2014). This chain of events from neural functions to strength and proprioception deficits and finally to reduced physical activity is of particular importance in light of growing evidence that reduced daily physical activity and regular exercise participation places individuals with ASD at greater risk for health problems, including obesity and additional comorbidities (Healy et al., 2019). Individuals with ASD may experience a vicious circle in which poor motor skills beget lower engagement in activity which further diminishes motor skills, etc. To combat this vicious circle, improving proprioception and encouraging individuals with ASD to engage in more physical activity is critical, as research with this population has shown that physical activity promotes angiogenesis and can increase vascular function in the motor cortex (Pereira et al., 2007) that, in combination with targeted training, may lead to improved motor skills. Future intervention studies with individuals with ASD might investigate (a) longitudinal rehabilitative training programs targeted at improving proprioceptive and strength deficits and/or (b) the relationship between increased physical activity and positive adaptations to the neuromuscular system in the form of improved strength and proprioceptive ability.

Limitations and Directions for Further Research

Among the limitations of this study, we conducted these tests in an environment that was unfamiliar to the participants. Although we took steps to maintain a closed, controlled laboratory environment, the environment may have inadvertently negatively affected the performance of participants with ASD who are known to prefer familiar repetitive experiences. Second, while we purposefully examined three positions and two speed-based tests of the ankle to include those commonly found during locomotion, future research will need to investigate higher and lower speed ranges, additional joints, and more complex tasks (i.e., bilateral and unilateral testing) in order to examine a more complete range of strength and proprioception skills. In addition, despite our efforts to provide participants verbal instructions and practice trials, the tasks we used might have posed particular difficulties for those with ASD. Third, our participants comprised only a small age-range of persons with ASD, and we did not require documentation regarding their level of support and/or a measured intelligence level. Future research should use a larger, more age diverse participant sample, and better describe the particular characteristics of participants with regard to their level of support and intelligence in order to better generalize these findings to others with ASD. We also did not require documentation or analyze developmental coordination disorder, sensory integration, or other comorbid conditions that may have further influenced outcomes variables. Future research should aim to include additional measures regarding these issues to denote possible interactions.

Conclusion

In summary, this study found that youth with ASD demonstrated reduced strength and proprioceptive capabilities when compared with age, sex, and BMI matched neurotypical controls. These findings lend support to the current literature regarding motor deficits of persons with ASD. While ASD is a complex diagnosis and requires attention from a myriad of aspects, it is apparent that rehabilitative programming aimed at improving lower extremity strength and proprioception has promise for important gains in motor functions and long term health.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was funded by the Jeffress Trust Awards in Interdisciplinary Research. Participants were compensated for their participation. The study sponsors were not involved in the study design, in the collection, analysis or interpretation of data; in the writing of the manuscript; or in the decision to submit the manuscript for publication.

ORCID iD

Hunter J. Bennett

Author Biographies

Cortney Armitano-Lago is a Postdoctoral Research Associate in the MOTION Science Institute at the University of North Carolina at Chapel Hill. Her research capitalizes on a complex system approach to quantify the interacting neurophysiological mechanisms that underlie human movement and lead to adaptive motor behaviors.

Hunter J. Bennett is an Assistant Professor and Director of the Neuromechanics Laboratory in the Department of Human Movement Sciences at Old Dominion University. His research interests span gait mechanics across many populations, including individuals with disabilities, and sports biomechanics.

Justin A. Haegele is an Associate Professor, and Director of the Center for Movement, Health, & Disability, in the Department of Human Movement Sciences at Old Dominion University. His research interests are situated in the interdisciplinary field of adapted physical activity, and focus on understanding the physical activity experiences of individuals with disabilities.

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