Functional Cortical Connectivity Related to Postural Control in Patients Six Weeks After Anterior Cruciate Ligament Reconstruction
21/07/2021
Lehmann T., Büchel D., Mouton C., Gokeler A., Seil R. and Baumeister J. (2021) Functional Cortical Connectivity Related to Postural Control in Patients Six Weeks After Anterior Cruciate Ligament Reconstruction. Front. Hum. Neurosci.15:655116. doi: 10.3389/fnhum.2021.655116
Introduction
Injuries to the anterior cruciate ligament (ACL) substantially affect knee joint laxity and cause long-term consequences for injured athletes. The accompanying functional impairments of an ACL tear thereby appear to extend beyond biomechanical alterations, comprising a loss of mechanoreceptors which consequently lead to diminished afferent input to higher levels of the sensorimotor system (Courtney et al., 2005; Kapreli et al., 2009). Although ACL injuries have repeatedly been shown to cause deficits in knee function even after surgical anterior cruciate ligament reconstruction (ACLR), knowledge about associated mechanisms of the sensorimotor system for compensating these functional impairments is still lacking (Ageberg, 2002).
A growing amount of evidence has begun identifying clinically meaningful neuroplastic changes in the sensorimotor system following ACL injury. Investigations utilizing transcranial magnetic stimulation, for instance, have detected enhanced motor thresholds in the ACL injured limb, whereas functional magnetic resonance imaging or electroencephalography (EEG) studies observed increased activations of the motor areas and lower activations of somatosensory areas in these patients (Neto et al., 2019). Along with altered somatosensory information from the ACL, decreased innervation to the primary sensory cortex (Valeriani et al., 1999), as well as different corticospinal and motor cortex excitability (Pietrosimone et al., 2015; Grooms et al., 2017; Lepley et al., 2020) have been observed in patients after ACL reconstruction. As a consequence of increased motor thresholds of the injured limb and decreased responsiveness of motor areas, greater cortico-cortical stimulation is required to evoke efferent neural signaling in the motor cortex for properly controlling motion and stability of the knee joint (Lepley et al., 2020). Thus, patients with ACL injury have been shown to recruit motor areas to a larger extent than healthy individuals, indicating that cortical adaptations may facilitate the restoration of lower limb motor functions by driving compensatory synergistic muscle patterns (Courtney et al., 2005). Whereas initial findings have identified compensatory cortical patterns in patients after ACLR during proprioceptive tasks (Baumeister et al., 2008, 2011), little is known about the cortical mechanisms behind the postural deficiencies in this population.
After ACLR and the following rehabilitation, many patients exhibit significantly decreased static postural stability as implied by increased center of pressure (CoP) excursions and velocities while standing on their injured limb (Lehmann et al., 2017). Although comprehensive evidence in the early postsurgical period is missing, postural stability in patients after ACLR was reported to deviate from both the preoperative level (Gokalp et al., 2016) and healthy controls (Parus et al., 2015) after the 4th and 8th week of surgery. With respect to these functional deficiencies in patients after ACLR, postural control reflects multimodal interactions within the sensorimotor system (Shumway-Cook and Woollacott, 2012). Recent findings from neuroimaging studies suggested that active contributions from the cortex continuously maintain and restore postural equilibrium (Wittenberg et al., 2017). Collectively, these EEG investigations demonstrated variations in power spectral density of theta (4–7 Hz), alpha-1 (8–10 Hz), and alpha-2 (10–12 Hz) frequency oscillations in frontal, motor, parietal, and occipital regions of the cortex. While it is suggested that theta band oscillations reflect a general brain integrative mechanism related to short term storage and manipulation of multimodal information for a given operation, alpha oscillations are related to the active inhibition of non-essential neuronal processing (Cheron et al., 2016), with alpha-1 reflecting global alertness of cortical areas and alpha-2 being associated with task-specific sensorimotor processing (Pfurtscheller and Lopes, 1999). Modulations of oscillatory activity during postural tasks therefore conceivably reflect direct or indirect interactions within complex transcortical and cortico-subcortical loops for detecting and counteracting postural instability (Wittenberg et al., 2017). The underlying functional relationships, as quantified by statistical interdependencies among distributed cortical regions, are referred to as functional connectivity (Friston, 2011). These connections show frequency-specific modulations within a fronto-parietal theta network and a parieto-occipital alpha network in response to postural instability and varying postural demands (Mierau et al., 2017; Varghese et al., 2019; Lehmann et al., 2020).
In the light of injury-related increased postural sway (Lehmann et al., 2017), patients after ACLR may require stronger interactions of functionally interconnected sensorimotor areas for properly controlling postural stability (Rosen et al., 2019; Jiganti et al., 2020), as well as hip and knee movement (Criss et al., 2020) while standing on the injured limb. Investigations of structural white matter changes following ACLR further indicated that the hemisphere contralateral to the injured leg may be particularly affected by this neurostructural reorganization (Lepley et al., 2020).
Therefore, the aim of the present case-control study is to explore leg dependent patterns of cortical connectivity related to postural control during single leg stances in patients 6 weeks following ACLR. It is hypothesized that patients after ACLR may show compensatory cortical mechanisms in terms of stronger functional connections within the theta and alpha networks compared to their matched controls. Furthermore, these cortical adaptations may specifically affect the stance on the injured limb. In this way, the current investigation may gain further insight into sensorimotor changes related to postural deficiencies after ACLR.