Lower extremity prism adaptation in individuals with anterior cruciate ligament reconstruction

Highlights

• Prism adaptation provides a means of investigating the organization of the sensorimotor system.

• Reconstructed individuals performed the task similar to controls when vision was perturbed.

• Reconstructed individuals able to effectively cross-calibrate sensory systems.

Abstract

Background

Emerging research has proposed a growing reliance on visual processing during motor performance in individuals following anterior cruciate ligament reconstruction. Reconstructed individuals display increased activation of visual processing areas during task execution and exhibit dramatic performance decrements when vision is completely removed, however the effect of visual information manipulation on performance remains unknown. The purpose of this study was to determine how manipulation of visual information changes performance in persons with anterior cruciate ligament reconstruction.

Methods

Twenty-one persons with anterior cruciate ligament reconstruction and 21 matched healthy adults reached to a target with the toe of the involved limb 50 times while wearing prism goggles that vertically shifted their visual field. Toe kinematics were collected to quantify endpoint error and reaching behavior.

Findings

Statistical analyses failed to detect significant differences, evidencing both groups performed similarly with respect to endpoint error, movement duration, peak and maximum endpoint velocities, and initial direction error.

Interpretation

When provided inaccurate information via a visual field perturbation, both groups demonstrated comparable adaptation and post-adaptation behavior. These results suggest this sample of persons with anterior cruciate ligament reconstruction are able to effectively integrate information across sensory systems as well as non-injured individuals.

Introduction

Current research suggests anterior cruciate ligament reconstructed (ACLR) individuals may redistribute the weighting of sensory faculties and rely more heavily on other afferent mechanisms such as visual feedback (Dingenen et al., 2015; Grooms et al., 2017; Grooms et al., 2018;Mohammadi Rad et al., 2012; Okuda et al., 2005). Indeed, ACLR individuals exhibit reduced postural control compared to controls when vision is removed during a static balance evaluation (Mohammadi Rad et al., 2012; Okuda et al., 2005), a dynamic transition from double- to single-leg balance (Dingenen et al., 2015), and a drop vertical jump (Grooms et al., 2018). Conversely, numerous studies have failed to identify significant group differences in task performance when visual feedback is removed (Akbari et al., 2016; Fridén et al., 1998; Harrison et al., 1994; Henriksson et al., 2001; Lion et al., 2018). Grooms et al., however, demonstrates altered cortical activity in regions responsible for sensory-visual spatial navigation despite similar biomechanical performance during a knee movement task (Grooms et al., 2017). Thus, it appears the method and severity (e.g. complete versus intermittent visual feedback) of visual feedback disturbance may also contribute to performance changes and the observed discordance of the existing literature.

While many studies have looked at the influence of visual feedback via complete visual allowance or removal (Akbari et al., 2016; Dingenen et al., 2015; Fridén et al., 1998; Harrison et al., 1994; Henriksson et al., 2001; Lion et al., 2018; Mohammadi Rad et al., 2012; Okuda et al., 2005), little research exists illustrating the effect of visual manipulation on performance in ACLR individuals (Grooms et al., 2018). Sarlegna and Sainburg state “completely removing information from a given modality may not provide accurate information about the relative contribution of that modality to the control process” (Sarlegna and Sainburg, 2009). Recently, Grooms et al. utilized strobe glasses to manipulate vision during a drop vertical jump and found knee flexion increased to a larger extent under stroboscopic visual feedback disruption in the ACLR group compared to controls (Grooms et al., 2018). Rather than granting vision or removing vision, evaluating performance when visual information is perturbed challenges the body to adapt to incomplete or inaccurate sensory feedback.

Prism adaptation has been widely accepted as a means of investigating and challenging the organization of the sensorimotor system, specifically it's visual and proprioceptive components (Held et al., 1966; Redding and Wallace, 1988). Prism lenses displace the visual field either laterally or vertically which creates a discord between visual and proprioceptive information, evident via movement error. Over consecutive trials, participants make adjustments to reduce error and realign visual and proprioceptive information (i.e. adapt) (Held et al., 1966). This paradigm targets an individual's ability to coordinate multiple components of the perceptual-motor system and cross-calibrate visual and proprioceptive afferent inputs to maintain spatial alignment (Redding and Wallace, 1988). Prism adaptation protocols have utilized upper extremity pointing and reaching tasks extensively, primarily to better understand and rehabilitate spatial neglect (Pisella et al., 2002; Rossetti et al., 1998) and study neural mechanisms associated with spatial realignment (Chapman et al., 2010; Luauté et al., 2009; Schintu et al., 2018). More recently, prism adaptation involving a lower extremity target has been investigated to assess transfer of adaptation between limbs (Morton and Bastian, 2004; Savin and Morton, 2008).

Prism adaptation involves two distinct mechanisms: strategic calibration and spatial realignment (Petitet et al., 2018; Redding and Wallace, 2002). The first is a fast process which is cognitively driven and results from a conscious correction to sensorimotor conflict between visual and proprioceptive information, while the second seeks to restore spatial mapping of the visual environment and occurs over a longer period of time. Strategic calibration is assessed during prism exposure whereas spatial alignment is assessed via aftereffects in the post-prism condition (Petitet et al., 2018; Redding and Wallace, 2002). In this primarily cerebellar-regulated process (Baizer et al., 1999; Block and Bastian, 2012; Hashimoto et al., 2015; Weiner et al., 1983), disjointed proprioception and visual information result in movement error which is modified over time to cohere visual and proprioceptive feedback. As mentioned before, alterations in the use of visual feedback coupled with injury to the lower limb (e.g. task effector for locomotion) could affect central nervous system processing, as well as sensory reweighting in the cerebellum, basal ganglia, and primary motor cortex (Ward et al., 2015). Previous applications of other adaptations paradigms found ACLR individuals exhibited altered adaptation performance (Roper et al., 2016; Stone et al., 2018). Thus, it stands to reason lower extremity prism adaptation may further elucidate sensorimotor integration abilities and biomechanical behavior in ACLR individuals.

Researchers may also select a specific prism paradigm to target certain aspects of adaptation. Availability of visual feedback during a movement trajectory can influence which sensory modalities are utilized during adaptation. Concurrent exposure provides visual feedback throughout the reach and at the endpoint whereas terminal exposure only provides visual feedback of endpoint location (Redding and Wallace, 1988). Terminal exposure is thought to compel participants to rely more on proprioceptive feedback during reaching since visual information is unavailable (Redding and Wallace, 1988; Uhlarik and Canon, 1971).

The purpose of this study was to determine how visual information manipulation changes performance during a lower extremity reaching task in ACLR individuals. We hypothesized ACLR individuals would be more reliant on visual information and take longer to reconcile the discord between visual and proprioceptive information. Further, we hypothesized that ACLR individuals would exhibit greater error during the first and second reach of prism adaptation compared to CON. When unperturbed visual feedback was provided, as was the case during baseline and post-exposure, we hypothesized performance would be similar between ACLR individuals and CON.