Neuroplasticity and Anterior Cruciate Ligament Injury

Abstract

Introduction:
Anterior cruciate ligament (ACL) tears are common, with a seemingly constant increase in their number, and potentially serious consequences for sports participation and long-term general and musculoskeletal health.

Areas of agreement:
Most players are able to return to cutting sport after ACL reconstruction, but some sustain further knee problems needing different approach to their rehabilitation.

Growing points:
Neurocognitive tasks, measuring reaction time, processing speed, visual memory and verbal memory, allow indirect assessment of cerebral performance. Situational awareness, arousal, and attentional resources may influence neurocognitive function, affecting the complex integration of vestibular, visual, and somatosensory information needed for neuromuscular control.

Areas of controversy:
The underlying reasons for uncoordinated, high-velocity movements observed during non-contact injuries of the knee producing an ACL tear are not well understood. Fundamental neuropsychological characteristics are responsible for situational awareness, sensory integration, motor planning, and coordination, all of which control joint stiffness. There is a strong link between acquisition of motor skills and neuronal plasticity at cortical and subcortical levels in the central nervous system; these links may evolve over time and engage different spatially distributed interconnected brain regions. A cascade of neurophysiological alterations occurs after ACL injury.

Areas timely for developing research:
Training can improve function; hence, rehabilitation programmes which include perturbation training, agility training, vision training and sport-specific skill training are essential after ACL injuries and for injury prevention, and to optimize return to play.

Full text

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Indian Journal of Orthopaedics
ISSN 0019-5413
Volume 54
Number 3
JOIO (2020) 54:275-280
DOI 10.1007/s43465-020-00045-2
Neuroplasticity and Anterior Cruciate
Ligament Injury
George Kakavas, Nikolaos
Malliaropoulos, Ricard Pruna, David
Traster, Georgios Bikos & Nicola
Maffulli

1 23
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Vol.:(0123456789)
1 3
Indian Journal of Orthopaedics (2020) 54:275–280
https://doi.org/10.1007/s43465-020-00045-2
REVIEW ARTICLE
Neuroplasticity andAnterior Cruciate Ligament Injury
GeorgeKakavas1· NikolaosMalliaropoulos2,3 · RicardPruna4· DavidTraster5· GeorgiosBikos8· NicolaMaulli3,6,7
Received: 14 November 2019 / Accepted: 13 January 2020 / Published online: 31 January 2020
© Indian Orthopaedics Association 2020
Abstract
Introduction Anterior cruciate ligament (ACL) tears are common, with a seemingly constant increase in their number, and
potentially serious consequences for sports participation and long-term general and musculoskeletal health.
Areas of agreement Most players are able to return to cutting sport after ACL reconstruction, but some sustain further knee
problems needing different approach to their rehabilitation.
Growing points Neurocognitive tasks, measuring reaction time, processing speed, visual memory and verbal memory,
allow indirect assessment of cerebral performance. Situational awareness, arousal, and attentional resources may influence
neurocognitive function, affecting the complex integration of vestibular, visual, and somatosensory information needed for
neuromuscular control.
Areas of controversy The underlying reasons for uncoordinated, high-velocity movements observed during non-contact
injuries of the knee producing an ACL tear are not well understood. Fundamental neuropsychological characteristics are
responsible for situational awareness, sensory integration, motor planning, and coordination, all of which control joint stiff-
ness. There is a strong link between acquisition of motor skills and neuronal plasticity at cortical and subcortical levels in
the central nervous system; these links may evolve over time and engage different spatially distributed interconnected brain
regions. A cascade of neurophysiological alterations occurs after ACL injury.
Areas timely for developing research Training can improve function; hence, rehabilitation programmes which include per-
turbation training, agility training, vision training and sport-specific skill training are essential after ACL injuries and for
injury prevention, and to optimize return to play.
Keywords Anterior cruciate ligament· Injury· Sensory input· Return to play· Neuroplasticity· Recovery
* Nicola Maffulli
n.maffulli@qmul.ac.uk
George Kakavas
info@fysiotek.gr
Nikolaos Malliaropoulos
contact@sportsmed.gr
Ricard Pruna
ricard.pruna@fcbarcelona.cat
David Traster
dr.traster@neurowellnessinstitute.com
Georgios Bikos
bikosg77@yahoo.gr
1 Fysiotek Spine & Sports Lab, Athens, Greece
2 Thessaloniki MSK Sports Medicine Clinic, Thessaloniki,
Greece
3 Queen Mary University ofLondon, Centre forSports
andExercise Medicine, London, UK
4 FC Barcelona, FIFA Medical Center ofExcellence, St Joan
Despi, Barcelona, Spain
5 Carrick Institute ofNeurology, CapeCanaveral, FL, USA
6 Department ofMusculoskeletal Disorders, School
ofMedicine andSurgery, University ofSalerno, Salerno,
Italy
7 School ofPharmacy andBioengineering, Guy Hilton
Research Centre, Keele University, Thornburrow Drive,
Hartshill, Stoke-on-TrentST47QB, England,UK
8 Euromedica Arogi Rehabilitation Center, Thessaloniki,
Greece
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276 Indian Journal of Orthopaedics (2020) 54:275–280
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Introduction
Anterior cruciate ligament (ACL) tears are common, with
a seemingly constant increase in their number in Major
League Soccer [1]. The injury carries potentially serious
consequences for sports participation and long-term health
[2]. The rate of ligament injuries in general, including
medial collateral ligament (MCL) injuries of the knee and
ankle sprains, has declined substantially in European pro-
fessional football during the past decade [3], but the actual
rate of development of ACL injuries is not known [4].
Several studies investigate return to play after ACL
injury and reconstruction, some of them documenting
successful early returns after ACL reconstruction, and
others starting to report that non-surgical management
is an option even in athletes. Most players do return to
cutting sport after ACL reconstruction, but some sustain
further knee problems and will need further surgery [5].
From a medical perspective, a subsequent knee injury or
the need of further knee surgery occurring in the final
phases of the rehabilitation period or early after return
to play are treatment failures [6]. The extent of this prob-
lem is, however, still unclear. In addition, although most
ACL-reconstructed male professional athletes can return
to players within 1year after surgery, their longer term
participation rate is unknown. [7].
We report evidence-based concepts on the connection
between neural mechanisms and ACL injury. Biomechani-
cal and neuromuscular characteristics are currently the pri-
mary focus of research on non-contact knee injury mecha-
nisms, as these risk factors are modifiable [8].
Clinical Implications forRehabilitation
andPrevention fromNeuroplasticity
Perspective
Neuroplasticity (or neural plasticity) refers to the ability
of central nervous system to adapt in response to extrinsic
(environmental) or intrinsic factors (e.g. an anatomically
defined lesion). These adaptations may involve alterations
to overall cognitive strategies, recruitment of different
neural circuits, or amplification or reduction of involve-
ment of certain connections or brain areas [9].
Neurocognitive tasks, such as those measuring reaction
time, processing speed, visual memory, and verbal mem-
ory, are well established in the neuropsychology literature
as indirect measures of cerebral performance [10]. Situ-
ational awareness, arousal, and attentional resources of the
individual may influence these areas of neuro-cognitive
function, affecting the complex integration of vestibular,
visual, and somatosensory information needed for neuro-
muscular control (Fig.1) [11].
The viscoelastic properties of muscle are continuously
adjusted depending on the anticipated functional demands
(e.g., landing, cutting, decelerating) [12, 13]. The neural ori-
gin of this ‘fine muscle tuning’ exerts a net effect on muscle
contractions that can increase joint stiffness tenfold, maxi-
mizing performance while preserving joint equilibrium and
stability. To optimize stiffness for each task, the surrounding
physical environment must be quickly modeled within the
brain before athletic maneuvers are actually executed. This
process is largely unconscious, and, in fact, conscious “over-
thinking” and inordinately high arousal levels may delay or
interrupt routine functional maneuvers [3].
Sports activities require situational awareness of a broad
attentional field to continuously monitor the surrounding
environment, filter irrelevant information, and simultane-
ously execute complex motor programs [14]. Increased
arousal or anxiety changes athletes’ concentration, narrows
their attentional field, and alters muscle activity, resulting in
poor coordination and inferior performance [15].
The neural computations that generate displayed strength
or injury risk movement profile are typically left out of the
return to play therapy, limiting our ability to improve the
patient’s chance to successfully pass the RTS criteria [16].
Rehabilitators need to better challenge the brain during train-
ing to transfer gains from the clinic to sports activity [17].
Following an ACL tear, the central nervous system may
increase its reliance on alternative sensory sources, such
as visual-feedback and spatial awareness [2]. One previous
investigation used neuroimaging to quantify brain activa-
tion differences between subjects with ACL deficiency who
did not return to previous levels of physical activity and a
healthy control group [11]. ACL-deficient subjects exhibited
increased activation in the posterior inferior temporal gyrus
(visual processing), pre-supplementary motor area (motor
planning), and secondary somatosensory area (pain and sen-
sory processing) [13].
The finding of depressed motor cortex excitability sug-
gests that greater motor cortex activation is required to
achieve motor drive and/or that motor cortex input from the
rest of the brain in the form of structural or functional con-
nectivity must increase to achieve motor drive [18].
Traditional rehabilitation encourages a focus of attention
on the knee with increased visual and cognitive knee posi-
tion control during movement training [17]. It is, therefore,
likely that differences in brain activation in part arise from
the rehabilitation process. The altered neuromuscular control
following ACL injury may induce chronic long-term neu-
roplastic changes associated with rehabilitation and motor
adaptations [19].
Alternatively, a direct approach to alter visual feedback
(blindfold, stroboscopic glasses, and virtual reality) during
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277Indian Journal of Orthopaedics (2020) 54:275–280
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rehabilitation may be beneficial to increase proprioceptive
sensory inputs, as opposed to increasing subjects’ reliance
on a visual-spatial neural strategy. [20].
Neuromuscular training that incorporates visual or neu-
rocognitive processing, such as ball tracking or engaging
other players, task complexity (reaction and decision-mak-
ing), anticipatory aspects, and cognitive load (dual task) can
address the possible sensory re-weighting of visual feedback
for motor control [21]. Research on ACL injury pathome-
chanics has greatly advanced, but the underlying reasons for
uncoordinated, high-velocity movements observed during
non-contact sprains are not well understood [22]. Fundamen-
tal neuropsychological characteristics are responsible for
situational awareness, sensory integration, motor planning,
and coordination [17], all of which control joint stiffness.
Therefore, they may also influence an individual’s injury-
avoidance strategy, regardless of sex [23].
The ACL may tear in less than 70ms [21], but the earli-
est reflexive activity for dynamic restraint requires at least
35ms to begin developing muscle tension [17]. Additionally,
cognitive appreciation of any coordination errors can take
up to 500ms [24]. Therefore, the high movement velocities
and forces associated with athletics require advanced cogni-
tive planning through feed-forward motor control; otherwise,
over reliance on reflexive strategies for dynamic stability
may be insufficient to protect the ACL. [25].
Increased physiological knee valgus, load reduced neu-
rocognitive function, increased joint laxity, small femoral
notch widths, and altered neuromuscular properties have
been considered as potential risk factors specific to young
females [11, 14, 15]. All these factors have warranted dis-
cussion as to potential interventions to target the relevant
processes. A further ACL injury following successful recon-
struction has been reported in up to 23% in athletes younger
than 25years when returning early to competitive sports
involving jumping and cutting activities [6]. Based on the
aforementioned continued neuromuscular control deficits,
traditional rehabilitation is not capable to restore normal
motor function in all patients after ACLR [12]. Compo-
nents of current rehabilitation programs entail a combina-
tion of exercises to increase muscle strength and endurance
and improve neuromuscular function. We acknowledge the
Fig. 1 Neuromuscular control
integration
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278 Indian Journal of Orthopaedics (2020) 54:275–280
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importance of addressing these factors: there is a clear need
for improvement in light of early development of osteoar-
thritis and second ACL injury risk [22].
Neuroplasticity Alterations After ACL
Reconstruction
Altered kinesthesia is common following ACL injuries [11].
Corrigan etal. measured both the ability to reproduce pas-
sive positioning and detect passive motion of the knee joint
in individuals with torn ACLs and age-matched controls
[26]. When compared to controls, those with ACL-deficient
knees exhibited significantly diminished ability to reproduce
passive positioning and to detect passive motion.
Surgical ACL reconstruction may enhance propriocep-
tion and kinesthesia by preserving afferents and regenerating
mechanoreceptors [27, 28].
Surgeries around the knee joint should preserve the integ-
rity of the knee’s mechanoreceptors and the afferent nerves
of its surrounding structures such as the capsule, collateral
ligaments, fat pad, synovium, and perimeniscal tissue [18].
The primary goal during surgery should be to save as much
sensory function as possible [29]. With the preservation or
restoration of the sensory function of the disrupted ligament,
symptoms such as functional instability and muscle weak-
ness may be avoided.
Despite intensive research in this area, the source and
the importance of the new population of mechanorecep-
tors within ACL surgical grafts are currently undetermined.
Receptors supplying the ACL graft may be restored by either
regrowth, regeneration, growth from the surrounding tissues,
dedifferentiation of other cells, or some other mechanism
[22]. Also, we do not know yet how these mechanoreceptors
actually function. Thus, the enhanced proprioception and
kinesthesia after ACL reconstruction may simply result from
enhanced functioning of other sensory receptors secondary
to the restoration of knee joint osteokinematics [16].
In football, external factors such as possession of the ball
and position of team mates and opponents are involved, and
are unpredictable [26]. The attentional and environmen-
tal components of neuromuscular function are largely not
addressed in current ACL rehabilitation programs. More
emphasis should be given to integrate sensory–visual–motor
control factors during rehabilitation such as reaction time,
information processing, and focus of attention, visual–motor
control, and complex-task–environmental interaction [30].
This is particularly important in the late stages of the reha-
bilitation process.
Finally, it should be mentioned that a patient tailored
rehabilitation programme is necessary for complete and
speedy recovery and return to sport. However, the prelimi-
nary stage to well-planned rehabilitation is accurate surgical
technique, starting with choice of the appropriate graft for
a given patient according to the sport they play. Also, it is
extremely important that the surgeon and the physiotherapy
team communicate constantly, as the rehabilitation process
may need to be adjusted according to the progress of the
patient. A goal- and task-oriented approach, instead of a
time limited and ‘cook book’ approach is necessary to obtain
maximum benefits, and restore full function.
Future Directions
These preliminary ideas may guide researchers to pursue
studies in several areas related to ACL injury prevention.
More data are needed to establish the precise periods of time
when individuals are vulnerable due to cognitive demands
such as sensory integration, decision-making, and motor
planning [3]. Sport-specific situations that may disrupt situ-
ational awareness in athletes can be explored, with particular
focus given to visual attention in high-intensity, dynamic,
complex environments. Unanticipated events can provoke a
universal startle response within the central nervous system
[13] resulting in a brief, involuntary, and widespread change
in neuromuscular activity. In terms of reliance on visual
information, athletes may suffer a brief episode of “inatten-
tional blindness” and fail to recognize important visual cues
simply, because they were not expecting them [20].
There is a strong link between acquisition of motor skills
and neuronal plasticity at cortical and subcortical levels
in the central nervous system that evolves over time and
engages different spatially distributed interconnected brain
regions [25]. Recent evidence indicates the large cascade of
neurophysiological alterations that occur after ACL injury
[31]. Although unilateral, an ACL injury induces bilateral
lower extremity dysfunction, with sensory information defi-
cits across the whole spectrum of the sensorimotor system,
lending further support to the theory of a neurophysiological
lesion [24].
Rehabilitation in patients after ACL injury should include
sensory challenges to decrease the dependency of patients
on visual information and facilitate neuroplasticity [19].
Patients may have ineffective motor-learning strategies and/
or motor learning to (re-) acquire motor skills may not be
sufficiently stimulated during traditional rehabilitation [18].
Such evidence could help to explain why patients do not
always regain motor skills after ACL injury, as the neuro-
plastic capacities may not be optimally challenged in cur-
rent rehabilitation programmes. Future research should aim
to: (a) evaluate larger samples of prospective ACL patients;
(b) include time between testing sessions, as well as other
ACL injury risk factors not collected as part of the present
study design including mental health challenges, current
medications and menstrual cycle as covariates to account
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279Indian Journal of Orthopaedics (2020) 54:275–280
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for potential confounding effects; (c) investigate changes in
connectivity within the S1 and cerebellar lobule XIIB fol-
lowing ACL prevention programs; (d) consider integrating
motor behavioral principles into ACL recovery and preven-
tion to explore their relative influence on brain function;
and (e) future investigations with larger sample sizes could
investigate whether our non-significant connectivity com-
parisons could provide any further insight on the cerebral
central nervous system contributions to ACL injury.
Given the reorganization of the central nervous system
that takes place after an ACL injury [12], we need to deter-
mine which principles of motor learning could enhance the
neuroplastic processes and translate to motor-learning inter-
ventions with the goal of optimal function of the patient.
Conclusion
Although its exact neurocircuits are not currently mapped
out, the ACL contributes to functional stability of the knee
joint by providing sensory feedback to the neuromuscu-
lar system [5]. Therefore, functional instability after ACL
injuries is likely secondary to both the loss of an impor-
tant mechanical restraint and a source of proprioception
and kinesthesia [25]. Neuromuscular training can improve
function; hence, rehabilitation programmes which include
perturbation training, agility training, vision training and
sport-specific skill training are essential after ACL injuries
and for injury prevention.
Future research should quantify musculoskeletal injury-
induced neuroplasticity, using more advanced motor-control
tasks, such as force or position matching or multi joint move-
ments, to improve the clinical applicability of these results.
Also, future research should focus on which, if any,
combinations of the presented novel motor-learning
principles yield better clinical outcomes. Motor learning
should be applied to support neuroplasticity after ACL
injury. Every individual and their brain are different: the
optimal solution may require motor-learning principles
individually tailored to each injured athletes.
Compliance with Ethical Standards
Conflict of interest The authors declare that there are no personal or
commercial relationships related to this study that would lead to a con-
flict of interest.
Ethical standard statement This article does not contain any studies
with human or animal subjects performed by any of the authors.
Informed consent For this type of study informed consent is not
required.
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