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Neurorehabilitation and brain stimulation studies of post-stroke patients suggest that action-observation effects can lead to rapid improvements in the recovery of motor functions and long-term motor cortical reorganization. Apraxia is a clinically important disorder characterized by marked impairment in representing and performing skillful movements [gestures], which limits many daily activities and impedes independent functioning. Recent clinical research has revealed errors of visuo-motor integration in patients with apraxia. This paper presents a rehabilitative perspective focusing on the possibility of action observation as a therapeutic treatment for patients with apraxia. This perspective also outlines impacts on neurorehabilitation and brain repair following the reinforcement of the perceptual-motor coupling. To date, interventions based primarily on action observation in apraxia have not been undertaken.
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PERSPECTIVE
published: 03 April 2019
doi: 10.3389/fneur.2019.00309
Frontiers in Neurology | www.frontiersin.org 1April 2019 | Volume 10 | Article 309
Edited by:
Giorgio Sandrini,
University of Pavia, Italy
Reviewed by:
Marianna Capecci,
Polytechnical University of Marche,
Italy
Marialuisa Gandolfi,
University of Verona, Italy
*Correspondence:
Mariella Pazzaglia
mariella.pazzaglia@uniroma1.it
Specialty section:
This article was submitted to
Neurorehabilitation,
a section of the journal
Frontiers in Neurology
Received: 30 August 2018
Accepted: 11 March 2019
Published: 03 April 2019
Citation:
Pazzaglia M and Galli G (2019) Action
Observation for Neurorehabilitation in
Apraxia. Front. Neurol. 10:309.
doi: 10.3389/fneur.2019.00309
Action Observation for
Neurorehabilitation in Apraxia
Mariella Pazzaglia 1,2
*and Giulia Galli 2
1Department of Psychology, University of Rome “La Sapienza,” Rome, Italy, 2IRCCS Fondazione Santa Lucia, Rome, Italy
Neurorehabilitation and brain stimulation studies of post-stroke patients suggest that
action-observation effects can lead to rapid improvements in the recovery of motor
functions and long-term motor cortical reorganization. Apraxia is a clinically important
disorder characterized by marked impairment in representing and performing skillful
movements [gestures], which limits many daily activities and impedes independent
functioning. Recent clinical research has revealed errors of visuo-motor integration in
patients with apraxia. This paper presents a rehabilitative perspective focusing on the
possibility of action observation as a therapeutic treatment for patients with apraxia. This
perspective also outlines impacts on neurorehabilitation and brain repair following the
reinforcement of the perceptual-motor coupling. To date, interventions based primarily
on action observation in apraxia have not been undertaken.
Keywords: apraxia, action recognition, action execution, mirror activity, neurorehabilitation
INTRODUCTION
Apraxia encompasses a broad spectrum of higher-order purposeful movement disorders (1) and
is most often associated with neurological damage to left-hemisphere (2). The accepted definition
of apraxia includes deficits in performing, imitating, and recognizing skilled actions involved in
the intentional movements, colloquially referred to as gestures (3). Pathological conditions such as
apraxia result from an inability to evince the concept of specific actions (4) or to execute related
motor programs (5). Classically, apraxia is diagnosed when a patient presents with an inability
to execute gestures in response to verbal commands or imitate with different effectors (mouth,
hand, or foot) (4), including movements involving the non-paretic limb ipsilateral to the lesion[s].
Although apraxia primarily affects motor activities, studies report that higher impairment levels
may be related to visuo-motor integration (6). Recent evidence supports the notion that apraxia
influences skilled acts in the environment, interferes with independent functioning, impedes daily
activities, and affects the performance of routine self-care (7,8); that is, persons may have difficulty
brushing their teeth (9), eating (7), preparing food (10), and getting dressed (11). As a consequence,
patients with apraxia can develop severe anxiety and reductions in the spontaneous use of social
gestures (12), leading to isolation and depression (13) and consequent delays in returning to
work (14).
Almost 50% of patients with left-hemispheric stroke (15) and 35% of patients with Alzheimer’s
disease and corticobasal degeneration (1618) develop apraxia that persists after illness onset
and affects functional abilities. Research to aid in the development and optimization of apraxia
neurorehabilitation is crucial. Several approaches for the treatment of apraxia deficits are currently
in practice [for a review see (19,20)], including verbal (21) or pictorial (22) facilitation and the
use of physical cues based on repetitive behavioral-training programs with gesture-production
exercises. The errorless completion method represents another recent approach (23). Autonomy in
Pazzaglia and Galli Neurorehabilitation and Apraxia
activities of daily living tends to be underestimated (24),
and rehabilitation studies remain limited due to the nature
of disturbances to automatic/voluntary dissociations (i.e., an
ability to execute actions only in natural settings). To date,
no rehabilitation treatment or therapeutic possibilities based
primary on action observation has been studied in apraxia.
THE VALUE OF ACTION OBSERVATION IN
TREATING APRAXIA
Language disorders among patients with apraxia who suffer from
concomitant aphasia suggest that defects in gesture imitation,
rather than gestures in response to verbal commands, are more
sensitive indicators of apraxia (25). Goldenberg has proposed
that imitation apraxia could be primarily considered a deficit of
perceptual analysis (26). Evidence from several studies indicates
that perceptual and motor codes are closely associated (27,
28) and that patients with apraxia may be defective both in
performing motor acts and in the perceptual code necessary to
represent the appropriate gesture. Sunderland and Sluman have
shown, for example, that problems orienting a spoon in a bean-
spooning task suggest an inability to remember the correct action
and to judge the correctness of the perceived action (29).
Although apraxia is commonly considered a motor
impairment, deficits in intact gestural perception are not
uncommon, occurring in 33% of one sample (30). Such
patients, who exhibit deficits in the execution of actions,
also commit errors when judging between correctly and
incorrectly performed acts (3032), understanding the meaning
of pantomimes (33,34), discriminating among action-related
sounds (35,36), matching photographs of gestures (26), engaging
visuo-motor temporal integration (6), and predicting incoming
observed movements (37,38).
Movement-execution effects in apraxia thus are not purely
motor processes and visual representations of given actions may
influence the actions’ execution by visuo-motor transfer (39). The
integrity of gesture representations has important implications
for rehabilitation strategies (40). The spatial and temporal use
of a body part for the planning of a tool-related action and
the imitation of others’ actions involve an inherent perceptual
component, which can be disturbed following apraxia onset. As
a result, modern assessments of apraxia include evaluations of
gesture understanding (32,41).
VISUAL-MOTOR STRATEGIES IN THE
REHABILITATION OF PATIENTS WITH
LIMB APRAXIA
The notion of common representations for both executed and
observed actions is of considerable interest in the applied field
of stroke neurorehabilitation (42,43). Despite the use of state-
of-the-art apraxia-evaluation batteries (44) to explore perceptual
deficits in the understanding of actions in patients with apraxia,
few studies have proposed new rehabilitation programs that
include elements of both observation and execution of actions.
Smania et al.’s (45) clinical examinations of 43 left brain-
damaged patients with apraxia revealed defective performances
in gesture execution and imitation, as well as in the recognition
and identification of transitive and intransitive gestures. For their
study, approximately half of the patients received training in
ecological action production and comprehension; the other half
underwent conventional language rehabilitation for the same
number of treatment hours. The training, which combined the
observation and execution of observed actions, consisted of three
progressive phases, each characterized by increasing degrees of
difficulty, obtained by phased reductions of facilitation cues as
performance improved. After 30 sessions, therapists recorded
significant improvements: approximately 50% improvement in
the ADL scale and an average of 40% in the praxis test (22). When
only considering apraxia patients with cortical lesions primarily
in the fronto-parietal network, the improvement was even greater
(45). No significant performance changes were observed in the
outcome measures of control patients who did not undergo
specific programs of gesture production/observation exercises.
Interestingly, authors reported a significant improvement in
gesture recognition performance after the apraxia treatment,
and a correlation was found between gesture comprehension
tests and the ADL questionnaire (ADL-gesture comprehension:
R=0.37, p=0.034) (22). These results suggest that the positive
effects of this rehabilitative approach in apraxia require parity
in the treatment of both the motor and the perceptual aspects
of action processing (45). Of note, beneficial effects persisted
for at least 2 months and extended to the daily living activities
even of untreated actions, helping patients attain functional
independence from their caregivers (22).
Goldenberg and Hagmann (9) developed a particularly
successful restorative method in which training comprised two
different methods. The first aimed at helping patients to learn and
correctly execute complete activities, with therapists providing
different support at all clinical steps (e.g., by demonstrating
gesture execution and asking patients to imitate them), and
reducing the support only when patients were able to perform
these steps on their own. The second aimed at directing patients’
attention to the functional meaning of objects’ individual features
and details, critical for various actions. This two-step procedure
ensured a double reinforcement of the action’s perceptual-
motor code: the first online within the simultaneity of the
demonstration and the second off-line as a delayed imitation.
The combination of these two methods led to significant
improvements in trained ADL, but virtually no generalization of
training effects was observed between trained and non-trained
activities. The therapy’s success was preserved among those
patients who performed the activities at home but not among
those who did not. In a subsequent study (46), the authors
developed a slightly different variant to previous approaches
in which patients carried out entire activities with a minimum
of errors. In this approach, the functional commonalities
between different objects were emphasized by providing verbal
instructions and visual and gestural support. Effects of these
treatments lasted up to 3 months after the treatment ended.
Compensatory treatment indicate that the patients showed
large improvements in ADL functioning after rehabilitative
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Pazzaglia and Galli Neurorehabilitation and Apraxia
programs aiming at teaching visual strategies to overcome the
apraxic impairments during execution of everyday activities (47).
Patients were taught strategies to compensate internally (e.g.,
self-verbalization or imagination) or externally (e.g., observation
of pictorial cues) the distinct phases of a complex action, while
performing the daily activities (4750).
All described interventions included elements of visuo-motor
integration and seemed to indicate that motor and visual
relearning in these patients was inextricably intertwined (see
Table 1).
Perceptual approach has been successfully applied to a
different rehabilitative intervention showing how action
observation has a positive effect on the performance of a specific
motor skill [for a review see (41,52,53)]. Patients watch a specific
motor act presented in a video clip or in a real demonstration,
and simultaneously (or thereafter) performed the same action.
A match (or mismatch) between visual signals and the gesture
performed drive re-learning about how the limb should move
in order to perform the motor act accurately (see Figure 1
for a hypothetical model on apraxia). Correctly reproducing
temporal (56,57), spatial (58), and body coding (59) helps
characterize movements, facilitate the motor patterns that
patients have to execute, and stimulate a rapid online correction
of movement (58,60,61). Observation combined with physical
practice in a congruent mode leads to increased motor cortex
excitability, and synaptic and cortical map plasticity strengthens
the memory trace of the motor act (62). Differently, rehabilitative
training based on physical practice alone (300–1,000 daily
repetitions) elicits only minimal neural reorganization (63). This
combined visual-motor therapy has been shown to improve
motor performance in patients that suffered a chronic stroke
(6486), patients with Parkinson’s disease (8792), children
with cerebral palsy (9397) and elderly individuals with reduced
cognitive abilities (98). Electrophysiological studies have also
reported positive effects of action observation on the recovery
of motor functions after acute and chronic stroke (71,99).
This non-invasive, inexpensive, user-friendly approach works
more quickly on biological effectors (mouth, limbs, and trunk),
promoting better and faster recovery.
A NEURAL SUBSTRATE FOR ACTION
OBSERVATION AND EXECUTION IN
APRAXIA REHABILITATION
The inextricable link between action perception and execution
was first posited in the ideomotor theory, which has been
validated through delineation of the brain network, known as
the mirror neuron system (MNS). Inspired by single-cell (“mirror
neuron”) recordings in monkeys (100,101), many neuroimaging
and neurophysiological studies have suggested that the adult
human brain is equipped with neural systems and mechanisms
that represent both the visual perception and execution of actions
in a common format (102). Action deficits among the patients
with apraxia may be described at multiple levels. While these
levels partially overlap, four levels of hierarchical modeling at
which an MNS mechanism can support an observed action
(42,103) are as follows:
(i) kinematic: Patients with apraxia frequently present with
abnormalities in kinematic movements in the form of motor
patterns that are slower, shorter, and less vertical than those
of individuals without apraxia (104);
(ii) motor: Limb apraxia interferes with the selection and
control of the hand-muscle activity (105). Moreover,
it interferes with the formation of appropriate hand
configurations for using objects (106);
(iii) goal: Understanding the immediate purpose of an action is
impeded; for example, patients with apraxia are impaired
access to mental representation of tool use (33);
(iv) intention: Patients present with an altered ability to monitor
the early planning phases of their own actions (107).
The cortical areas have been shown to contain mirror neurons
that are often described as a part of an integrated sensorimotor
information system underpinned by neural activity in the frontal
(103), parietal (108), and superior temporal sulcus areas. This
system is called the action observation network (AON) (109).
In humans, these cortical regions mediate the observation of
actions that form a part of the observer’s motor repertoire (41).
They also contribute to the imitation (110) and comprehension
(111) of these movements, and are involved in skill acquisition
(112). Lesion symptom mapping studies have reported gestural
deficits in patients with apraxia, which are most frequently
apparent following lesions in the inferior frontal lobe (30,113
116), and in supramarginal and angular gyrus (37,113,115,
117) of the left hemisphere. However, apraxia has also been
observed in patients with damage in posterior middle temporal
lobe, anterior temporal lobe (37,113,115,117), occipital, and
subcortical regions (6,118,119). Despite the damaged neural
substrate was not constant across all the studies, it includes the
areas that are considered crucial for the AON. Undoubtedly, the
mirror neurons just provide a part of the complex information
for achieving action comprehension while action recognition
and production occur simultaneously by accessing the same
neural representations. However, as posited by the influential
cognitive neuropsychological models of apraxia (120,121) and
demonstrated by various clinical studies (121124), the range
of possible dissociations between action execution and action
understanding that can occur in patients with apraxia is quite
multifaceted and cannot be explained by a mere action mirroring
mechanism nor by a single lesion locus. Impairments in the
visual recognition of action paralleled deficits in performing
these actions could depend on both common and distinct
neural localization, most of which could be external to mirror
regions. Failures in imitating or in recognizing gestures may
occur because of damage at any level in the process between
perceiving (input lexicon) and performing (output lexicon) an
action (120,121). Indeed, some apraxic patients show deficits
in the recognition/discrimination of the gestures, some do not
[for a review (125)]. Theoretical and empirical studies suggest
that complementary routes to action understanding taking place
on the dorso-dorsal and ventro-dorsal stream (126,127). Lesion
in ventral-dorsal stream may impede the top-down activation
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Pazzaglia and Galli Neurorehabilitation and Apraxia
TABLE 1 | Apraxia intervention studies.
References Number of participants Treatment
duration
Type of
action
Control Intervention Perceptual aspects
of training
Improvements in
experimental group
No effect
Experimental
group
Control
group
van Heugten
et al. (47)
33 30 min for 12
weeks
Everyday
activities
Strategy training Observation of picture
sequences Imagination
ADL Barthel Index
Apraxia Test Motor
functioning
Goldenberg and
Hagmann (9)
15 5 weeks Three
activities from
the domains
eating,
dressing, and
grooming
Direct training of
the activity:
errorless
completion of the
activity
The patients perform
action immediately after
observing the
therapist’s
demonstration
10 patients improved
on all three trained
activities
6 months later,
improvement is
not maintained
without practice
Smania et al. (45) 6 7 35 sessions,
three per
week
Transitive
action
Intransitive
action
Imitation
Aphasia
therapy
Gesture
recognition
Gesture execution
Observation of picture
(context, object)
Gesture recognition
Imitation
Apraxia Test Gesture
recognition
Verbal
comprehension
Oral apraxia
Donkervoort et al.
(48)
42 48 8 weeks Everyday
activities
Occupational
therapy
Strategy training Observation of picture
sequences Imagination
ADL Barthel Index Apraxia Test ADL
untrained
Goldenberg et al.
(46)
6 4 weeks Four everyday
activities
Explorative training
vs. Direct training
of the activity
The patients perform
action immediately after
observing the
therapist’s
demonstration
Direct training of activity
reduced errors and
amount of assistance
Exploration
training had no
effect on
performance
Smania et al. (22) 18 15 30 sessions,
three per
week
Transitive
action
Intransitive
action
Imitation
Aphasia
therapy
Gesture
recognition
Gesture execution
Observation of picture
(context, object)
Gesture recognition
Imitation
Apraxia Test Gesture
recognition ADL
Verbal
comprehension
Oral apraxia
Geusgens et al.
(50)
56 57 25 sessions,
8 weeks
Action of daily
living
Occupational
therapy
Strategy training Observation of picture
sequences
ADL untrained
Geusgens et al.
(49)
29 25 sessions,
8 weeks
Action of daily
living
Strategy training Observation of picture
sequences
Apraxia Test ADL
trained ADL untrained
Barthel Index
Functional Motor
Test
Bolognini et al.
(51)
6 6 3 sessions,
10 min
Limb gesture
imitation
Sham
stimulation
Anodal tDCS on
the left parietal
cortex
Imitation (observation
+execution)
Imitation execution tDCS on the motor
cortex
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Pazzaglia and Galli Neurorehabilitation and Apraxia
FIGURE 1 | Hypothetical model for performing and recognizing a transitive action [adapted from (54) and (55)]. Failures in performing or recognizing gestures may
occur because of damage at any stage in the directional flow between perceiving (input) and performing (output) the action. The observation of a video clip or a real
demonstration of action can have a positive effect on the selection and retrieval of the correct movement. In figure the example of grasping a cup of coffee. After the
correct visual identification of the object as a cup, patients with apraxia have a difficult retrieval of the correct action associated with that object. When an incorrect
movement is performed, a discrepancy occurs between the (correct) action observed on the model and the perception of own (incorrect) performed gesture.
Combining motor training and action observation may enhance the relearning of daily actions and strengthen the visuo-motor coupling.
of motor engrams. It may produce disturbances in the on-
line selection and integration of distinctive and relevant motor
acts that ensure a high recognizability of the gesture (117).
This can be responsible for the disordered motor planning,
imitation, and motor-memory recall of gesture movements found
in patients with apraxia (126,127). As has been briefly shown,
many questions remain, and there may be more than one
mechanism leading to apraxia disturb. Given the complexity
of the impairment and the separate neural substrates that
are typically affected in apraxia, treatments related to action
observation to support action execution or relearning of gestures
of daily living, can be planned.
NEUROREHABILITATION AND BRAIN
REPAIR AFTER APRAXIA
The behavioral success of rehabilitation methods based on the
principle of action observation should promote reorganization
by adaptive plasticity at the neural level (128,129). Functional
reorganization clearly depends on the residual neural integrity
of efferent (motor) and afferent (sensory) information, which
leads to improved treatment outcomes among some apraxia
patients but not for others. In this perspective, we considered
three possible sources of informational content for how
neurorehabilitation and brain repair after apraxia works: injury
site, elapsed time after apraxia onset, and lesion size.
The first factor to consider is the location of the infarct,
which can ultimately determine the outcome of rehabilitation
treatment. Whereas, lesions of the frontal and parietal cortices
in the left hemisphere have been shown to primarily disrupt
gesture production in patients with apraxia (2), no clear
correlation has been found between lesion location and
impairment in visual gesture representation. Apraxic patients
with cortical lesions—but not those with subcortical lesions—
cannot comprehend the meaning of gestures (130). In rare
cases, a lesion in the left occipito-temporal cortex may also
critically hamper the ability to recognize gestures in patients
with apraxia (120,131). Patients with parietal lesions have also
been reported to exhibit significant impairments in executing
gestures but only slight impairments in understanding those
performed by others (132). The neural specificity of this
disturbed typology may explain why certain patients with
apraxia are able to comprehend the meaning of gestures
despite being unable to perform them themselves. Accordingly,
single-case and group studies report dissociations between
action execution and representation and the underpinning
damaged neural substrate (121124). Efficiency and speed of
the therapeutic means of action observation depend partly
on the different roles that intact and damaged brain regions
play in both action production and recognition (125,133).
Neural damage to a functional system can be partial, and
studies in monkeys seem to suggest that the frontal and
parietal cortices are neurally equipped for such divisions of
labor (134).
Several studies have documented that neurorehabilitation
techniques involving observation strategies among brain-
damaged patients induce long-lasting neural changes in the
motor cortex, potentiating activity in the affected areas. In
brain-damaged patients, TMS studies have found direct evidence
of increased motor-cortex excitability (84), and synaptic and
cortical map plasticity have been documented using fMRI (75).
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Pazzaglia and Galli Neurorehabilitation and Apraxia
TMS studies have also indicated that action observation alone
is able to drive reorganization in the primary motor cortex,
strengthening the motor memory of observed actions among
young (135) and elderly subjects (mean ages: 34 and 65 years,
respectively) (98) and among chronically brain-damaged patients
(84). Additionally, a study reported positive effects on gesture
imitation of anodal transcranial direct current stimulation
(tDCS) on the left parietal compared to sham tDCS, supporting
the view that apraxia disorders in Parkinson (136) and in brain
left damaged patients (51) can be improved by stimulating
distinct structures.
A second factor to consider is the temporal stage of the illness.
The neural substrates of action production and comprehension
could be associated with different physiological mechanisms at
different temporal stages of apraxia. Frontal and parietal areas
may become temporarily inactive because of cerebral edema
and intracranial hypertension, hemodynamic signs of ischemic
penumbra, or local inflammatory effects in acute but not chronic
stages of apraxia (137). Different studies report that during
early periods (including an acute four-week, post-onset phase),
impaired gesture recognition may be associated with left frontal–
lobe and basal-ganglia lesions (138), whereas in the chronic stages
of the illness, these deficits can be associated with left-parietal
lesions (32,37).
In practice, transitory effects such as the inability to mimic
actions from visual cues are often observed in apraxia’s early
stages. If so, an observation intervention in early therapy may
be inefficacy.
During later apraxia stages, a close overlap of the networks
underlying observation and execution, as indicated by advanced
neuroimaging and the lesion locations studies in patients, are
helpful in identifying patient in which observative approach
is potentially useful. Observation therapy associated with
adaptive neurophysiological and neurometabolic changes can be
conducted even several years after stroke onset. A session of 4
weeks of active, 18 days-cycle visual/motor training has been
found to significantly enhance motor function, with increases
in the activity of specific motor areas that possess mirror
properties (75). Massed, high-frequency rehabilitative training
(300–1,000 daily repetitions) is needed to elicit minimal neural
reorganization (63). These increases in cortical activity during
both action observation and execution also tend to be present
in the hemispheres (139,140) close to and far from the
lesion site.
A third possible factor to consider is that the failure to link
perceptual and motor representations in apraxia treatment may
be an effect of infarct size; larger lesions are more likely to include
front parietal injury and may not benefit from observation
treatment. Indeed, improvements in imitation (reproduction
off-line of the observed gesture) in patients with apraxia are
influenced by the size of the parietal lesion (51): the larger
the left parietal damage, the smaller the tDCS treatment-related
improvement. When a functional system is completely damaged,
however, recovery is achieved largely by process of substitution
and may depend on the implicit engagement of neural systems to
take over the functions of the damaged areas (141).
Whereas, some systems may constitute the sites of gesture
performance, others may reduce the impact of deficits (142)
by stimulating coupled visual knowledge mechanisms (98). The
integrity of both the frontal and parietal cortices might be crucial
for re-learning as a result of motor mirroring. Nonetheless, non-
injured cortical areas could also trigger additional, independent
internal mechanisms that support but are not necessary for
guiding the motor system to match vision with motor routines
(143,144). Studies on the neural representations of motor skills
based on observations of the motor cortex of macaque monkeys
(145) and humans (146) provide empirical support for such
an alternative system. These studies suggest that congruent
activity during action execution/observation occurs even outside
the canonical “mirror area,” representing a potential general
property of the motor system. Targeting interventions on the
basis of specific brain structures intact and damaged that could
mediate the effects of training is an important future challenge in
cognitive neurorehabilitation.
CONCLUSION
While research on the relationship between observed and
executed actions in apraxia neurorehabilitation has a short
history, it has already provided insights about the positive effect
of a visual-motor training. The observation of actions through
a process of visual retrieval may help in the selection of the
most probable action, providing a powerful tool for overcoming
intentional motor-gestural difficulties (55). Moreover, tailored
interventions based on individual’s ability to acquire new (or
relearn old) motor-memory traces through multisensory [i.e.,
auditory (35,147), olfactory (148,149), and tactile (150
155)] feedback may be the most promising approach for a
normal temporal integration action (156,157). Multisensory
stimulation can activate multiple cortical brain structures,
inducing cortical reorganization and modulating motor cortical
excitability for the stimulated afferents (158,159). Results
are encouraging, but it is important to emphasize that this
hypothesis does not imply that all deficits in apraxia can
be treated by action observation therapy. Rather, we believe
that action observation might be a therapeutic option for
improving praxis function among certain specific typologies
of patients.
AUTHOR CONTRIBUTIONS
MP: study concept and design, manuscript development, and
writing. GG: contributed to the writing of the manuscript.
FUNDING
This work was supported by the Italian Ministry of Health
(RF-2018-12365682 to MP).
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Pazzaglia and Galli Neurorehabilitation and Apraxia
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Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2019 Pazzaglia and Galli. This is an open-access article distributed
under the terms of the Creative Commons Attribution License (CC BY). The use,
distribution or reproduction in other forums is permitted, provided the original
author(s) and the copyright owner(s) are credited and that the original publication
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distribution or reproduction is permitted which does not comply with these terms.
Frontiers in Neurology | www.frontiersin.org 10 April 2019 | Volume 10 | Article 309
... Sensorimotor representations are also essential for building and maintaining corporeal awareness. Indeed, not only does the mere motor imagination (MI) of an action enhance the motor representation of the imagined action [25], but the mere motor experience of a particular action can also enhance its representational organization [26]. ...
... These findings could be relevant in cases in which the sense of agency changes according to the sensorimotor deficit severity and paretic upper limb activity [34] or, for example, in apraxia [35]. These stimulating results enhance our knowledge and interest for further basic and clinical investigations on the role of body and action in clinical and rehabilitation [26,[36][37][38]. ...
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Our bodily experience arises primarily from the integration of sensory, interoceptive, and motor signals and is mapped directly into the sensorimotor cortices [...]
... 2 However, there are few reports about the rehabilitation benefit in iNPH patients after shunt surgery. 2 Action observation (AO) has become a unique rehabilitation tool to date for both neurological and non-neurological disorders. [19][20][21][22][23] AO is based on the mirror neuron system (MNS), used in the rehabilitation program to recover motor control and learning by recruiting the neural structures that can perceive and execute the actions. 19 Mirror neurons can be responsible for the mechanism linking to observing the action and its understanding and imitation. ...
... 29 AO has usually been used and demonstrated to be of benefit for improving motor function and learning in several conditions. [19][20][21][22][23][24]26,28,[30][31][32][33][34] It can be practiced by observing the action alone (action observation; AO) or observing combined with movement execution (action observation-execution; AOE). From a recent study by Zhu et al. 35 that investigated the effect of AO and AOE on motor-cortical activation using magnetoencephalography in stroke patients. ...
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Objective: This study aimed to investigate the feasibility of AO in iNPH patients. Methods: A single-group pretest-posttest design was conducted in twenty-seven iNPH patients. Gait and mobility parameters were assessed using the 2D gait measurement in the timed up and go (TUG) test for two trials before and after immediate AO training. The outcomes included step length and time, stride length and time, cadence, gait speed, sit-to-stand time, 3-m walking time, turning time and step, and TUG. In addition, early step length and time were measured. AO consisted of 7.5 min of watching gait videos demonstrated by a healthy older person. Parameters were measured twice for the baseline to determine reproducibility using the intraclass correlation coefficient (ICC3,1). Data between before and after immediately applying AO were compared using the paired t-test. Results: All outcomes showed moderate to excellent test-retest reliability (ICC3,1=0.51 0.99, p<0.05), except for the step time (ICC3,1=0.19, p=0.302), which showed poor reliability. There were significant improvements (p<0.05) in step time, early step time, gait speed, sit-to-stand time, and turning time after applying AO. Yet, the rest of the outcomes showed no significant change. Conclusions: A single session of AO is feasible to provide benefits for gait and mobility parameters. Therapists may modify this method in the training program to improve gait and mobility performances for iNPH patients.
... AO therapy shows a "topdown" effect in neurorehabilitation by activating the MSN and causing a reorganization of motor representations at the central level (14). So far, AO therapy has been successfully applied to the rehabilitation of motor function for stroke patients, children with cerebral palsy, and individuals suffering from Parkinson's disease (22)(23)(24). ...
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Objective This study aimed to investigate brain plasticity by somatosensory stimulation (SS) and sensory observation (SO) based on mirror neuron and embodied cognition theory. Action observation therapy has been widely adopted for motor function improvement in post-stroke patients. However, it is uncertain whether the SO approach can also contribute to the recovery of sensorimotor function after stroke. In this study, we explored the therapeutic potential of SO for sensorimotor dysfunction and provided new evidence for neurorehabilitation.Methods Twenty-six healthy right-handed adults (12 men and 14 women), aged 18–27 (mean, 22.12; SD, 2.12) years were included. All subjects were evaluated with task-based functional magnetic resonance imaging (fMRI) to discover the characteristics and differences in brain activation between SO and SS. We adopted a block design with two conditions during fMRI scanning: observing a sensory video of brushing (task condition A, defined as SO) and brushing subjects' right forearms while they watched a nonsense string (task condition B, defined as SS). One-sample t-tests were performed to identify brain regions and voxels activated for each task condition. A paired-sample t-test and conjunction analysis were performed to explore the differences and similarities between SO and SS.ResultsThe task-based fMRI showed that the bilateral postcentral gyrus, left precentral gyrus, bilateral middle temporal gyrus, right supramarginal gyrus, and left supplementary motor area were significantly activated during SO or SS. In addition to these brain regions, SO could also activate areas containing mirror neurons, like the left inferior parietal gyrus.ConclusionSO could activate mirror neurons and sensorimotor network-related brain regions in healthy subjects like SS. Therefore, SO may be a promising novel therapeutic approach for sensorimotor dysfunction recovery in post-stroke patients.
... Around one-third of people with SCI experience persistent and severe pain, with NP being the most prevalent type, occurring in up to 96% of patients [18,19]. NP typically manifests within the first year following SCI [20], is resistant to nonpharmacologic interventions such as surgery, neurostimulation, and physical and psychological therapy [21][22][23][24], and is associated with increased drug prescriptions and health care provider visits [25]. Since NP has a negative impact on a patient's daily activities, quality of life, mood, and rehabilitation outcome, the Food and Drug Administration (FDA) has approved a variety of drugs and pharmacological treatments for NP [26][27][28]. ...
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Neuropathic pain (NP) is a common chronic condition that severely affects patients with spinal cord injuries (SCI). It impairs the overall quality of life and is considered difficult to treat. Currently, clinical management of NP is often limited to drug therapy, primarily with opioid analgesics that have limited therapeutic efficacy. The persistence and intractability of NP following SCI and the potential health risks associated with opioids necessitate improved treatment approaches. Nanomedicine has gained increasing attention in recent years for its potential to improve therapeutic efficacy while minimizing toxicity by providing sensitive and targeted treatments that overcome the limitations of conventional pain medications. The current perspective begins with a brief discussion of the pathophysiological mechanisms underlying NP and the current pain treatment for SCI. We discuss the most frequently used nanomaterials in pain diagnosis and treatment as well as recent and ongoing efforts to effectively treat pain by proactively mediating pain signals following SCI. Although nanomedicine is a rapidly growing field, its application to NP in SCI is still limited. Therefore, additional work is required to improve the current treatment of NP following SCI.
... It proposes that it is advantageous to consider somatotopically head, upper-limb, and lower limbs body areas for focal stimulation, to boost the sense of embodiment and agency in body parts with reduced access to sensori-motor information [89]. Yet, this may produce positive residual responses, improving the effects of treatment rehabilitative [90,91]. ...
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Spinal cord injuries (SCI) are disruptive neurological events that severly affect the body leading to the interruption of sensorimotor and autonomic pathways. Recent research highlighted SCI-related alterations extend beyond than the expected network, involving most of the central nervous system and goes far beyond primary sensorimotor cortices. The present perspective offers an alternative, useful way to interpret conflicting findings by focusing on the deafferented and deefferented body as the central object of interest. After an introduction to the main processes involved in reorganization according to SCI, we will focus separately on the body regions of the head, upper limbs, and lower limbs in complete, incomplete, and deafferent SCI participants. On one hand, the imprinting of the body’s spatial organization is entrenched in the brain such that its representation likely lasts for the entire lifetime of patients, independent of the severity of the SCI. However, neural activity is extremely adaptable, even over short time scales, and is modulated by changing conditions or different compensative strategies. Therefore, a better understanding of both aspects is an invaluable clinical resource for rehabilitation and the successful use of modern robotic technologies.
... Motor imagery is a promising technique for motor rehabilitation [93,106,107] and can enhance the effects of VR activities, increasing the sense of embodiment and favoring adaptive plasticity. Its effects on motor function have been attributed to the strengthening of motor programs [93,108,109], while its effects on pain remain unclear. It has been hypothesized that the production of motor imagery may influence the interaction among mental representations of the body, nociception, sensorimotor integration, and pain [110,111]. ...
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Neuropathic pain (NP) is a chronic, debilitating, and resistant form of pain. The onset rate of NP following spinal cord injuries (SCI) is high and may reduce the quality of life more than the sensorimotor loss itself. The long-term ineffectiveness of current treatments in managing symptoms and counteracting maladaptive plasticity highlights the need to find alternative therapeutic approaches. Virtual reality (VR) is possibly the best way to administer the specific illusory or reality-like experience and promote behavioral responses that may be effective in mitigating the effects of long-established NP. This approach aims to promote a more systematic adoption of VR-related techniques in pain research and management procedures, highlighting the encouraging preliminary results in SCI. We suggest that the multisensory modulation of the sense of agency and ownership by residual body signals may produce positive responses in cases of brain-body disconnection. First, we focus on the transversal role embodiment and how multisensory and environmental or artificial stimuli modulate illusory sensations of bodily presence and ownership. Then, we present a brief overview of the use of VR in healthcare and pain management. Finally, we discus research experiences which used VR in patients with SCI to treating NP, including the most recent combinations of VR with further stimulation techniques.
... For example, studies using rats have demonstrated that tactile therapy along with invasive vagal stimulation can lead to the reorganization of the primary sensory cortex, thus improving sensory function [61]. Similarly, this stimulation allows the better recovery of motor functions-particularly for movements of the upper limbs-if associated with motor training, compared to rehabilitation alone [62][63][64]. The transient brain response evoked by each heartbeat plays a role in cognitive functions that are usually studied separately, such as body perception, self-related cognition, and spatio-temporal evolution of dynamic visual events [65]. ...
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Spinal cord injuries (SCIs) exert devastating effects on body awareness, leading to the disruption of the transmission of sensory and motor inputs. Researchers have attempted to improve perceived body awareness post-SCI by intervening at the multisensory level, with the integration of somatic sensory and motor signals. However, the contributions of interoceptive-visceral inputs, particularly the potential interaction of motor and interoceptive signals, remain largely unaddressed. The present perspective aims to shed light on the use of interoceptive signals as a significant resource for patients with SCI to experience a complete sense of body awareness. First, we describe interoceptive signals as a significant obstacle preventing such patients from experiencing body awareness. Second, we discuss the multi-level mechanisms associated with the homeostatic stability of the body, which creates a unified, coherent experience of one’s self and one’s body, including real-time updates. Body awareness can be enhanced by targeting the vagus nerve function by, for example, applying transcutaneous vagus nerve stimulation. This perspective offers a potentially useful insight for researchers and healthcare professionals, allowing them to be better equipped in SCI therapy. This will lead to improved sensory motor and interoceptive signals, a decreased likelihood of developing deafferentation pain, and the successful implementation of modern robotic technologies.
... motor representations (Cho & Proctor, 2013;Wilf, Holmes, Schwartz, & Makin, 2013). In our task, the congruency effect was not specified by the handle of a cup, but rather by its position being upright or down, which would habitually elicit a supinated or pronated grasp, respectively (Pizzamiglio et al., 2020;Pazzaglia & Galli, 2019;Rounis et al., 2017;Herbort & Butz, 2011). Previous studies have demonstrated hand-object compatibility effects differ according to whether the object location is centered (Bub et al., 2018;Cho & Proctor, 2013). ...
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Selecting hand actions to manipulate an object is affected both by perceptual factors and by action goals. Affordances may contribute to “stimulus–response” congruency effects driven by habitual actions to an object. In previous studies, we have demonstrated an influence of the congruency between hand and object orientations on response times when reaching to turn an object, such as a cup. In this study, we investigated how the representation of hand postures triggered by planning to turn a cup was influenced by this congruency effect, in an fMRI scanning environment. Healthy participants were asked to reach and turn a real cup that was placed in front of them either in an upright orientation or upside–down. They were instructed to use a hand orientation that was either congruent or incongruent with the cup orientation. As expected, the motor responses were faster when the hand and cup orientations were congruent. There was increased activity in a network of brain regions involving object-directed actions during action planning, which included bilateral primary and extrastriate visual, medial, and superior temporal areas, as well as superior parietal, primary motor, and premotor areas in the left hemisphere. Specific activation of the dorsal premotor cortex was associated with hand–object orientation congruency during planning and prior to any action taking place. Activity in that area and its connectivity with the lateral occipito-temporal cortex increased when planning incongruent (goal-directed) actions. The increased activity in premotor areas in trials where the orientation of the hand was incongruent to that of the object suggests a role in eliciting competing representations specified by hand postures in lateral occipito-temporal cortex.
... Currently, different approaches were used to treat apraxia deficits, including strategy training (Donkervoort et al., 2001), gesture training (Smania et al., 2006), verbal (French et al., 2009), graphic facilitation (Smania et al., 2006), the practice of physical cues based on the repetitive behavioraltraining programs with the gesture-production activities, and the errorless completion method (Buxbaum et al., 2008). However, to date, independence in the activities of daily living tends to be underestimated (Etcharry-Bouyx et al., 2017), and rehabilitation evidence remains insufficient due to the nature of disturbances to the automatic voluntary dissociations (Pazzaglia & Galli, 2019). A previous systematic review by Lindsten-McQueen et al. (2014) demonstrated the beneficial influences of the apraxia treatment in patients with various neurological disorders. ...
Article
Apraxia is widely used to describe one of the more disabling deficits following left strokes. The role of rehabilitation in treating apraxic stroke patients remains unclear. This systematic review was conducted to study the impacts of various rehabilitation interventions on the limb apraxia post-stroke. PubMed, SCOPUS, PEDro, CINAHL, MEDLINE, REHABDATA, and Web of Science were searched for the experimental studies that investigated the effects of the rehabilitation interventions on apraxia in patients with stroke. The methodological quality was rated using the Physiotherapy Evidence Database scale (PEDro). Six studies met our inclusion criteria in this systematic review. Four were randomized controlled trials, pilot (n= 1), and case study (n= 1). The scores on the PEDro scale ranged from two to eight, with a median of seven. The results showed some evidence for the effects of strategy training and gesture training interventions on the cognitive functions, motor activities, and activities of daily livings outcomes poststroke. The preliminary findings showed that the effects of the strategy training and the gesture training on apraxia in patients with stroke are promising. Further randomized controlled trials with long-term follow-ups are strongly needed.
... Indeed, research on the relationship between observed and executed actions in apraxia neurorehabilitation has provided insights about the positive effect of a visualmotor training. 26 Also, positive effects of Virtual Reality (VR) in neurorehabilitation are recently investigated, about increasing repetition, engagement and motivation during rehabilitation sessions. VR systems are effective in supporting feedback, have the capability adapt to individual needs, can deliver high intensity and meaningful repetitive exercises to encourage motor control and motor learning. ...
Article
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Background: Buccofacial Apraxia is defined as the inability to perform voluntary movements of the larynx, pharynx, mandible, tongue, lips and cheeks, while automatic or reflexive control of these structures is preserved. Buccofacial Apraxia frequently co-occurs with aphasia and apraxia of speech and it has been reported as almost exclusively resulting from a lesion of the left hemisphere. Recent studies have demonstrated the benefit of treating apraxia using motor training principles such as Augmented Feedback or Action Observation Therapy. In light of this, the study describes the treatment based on immersive Action Observation Therapy and Virtual Reality Augmented Feedback in a case of Buccofacial Apraxia. Participant and methods: The participant is a right-handed 58-years-old male. He underwent a neurosurgery intervention of craniotomy and exeresis of infra axial expansive lesion in the frontoparietal convexity compatible with an atypical meningioma. Buccofacial Apraxia was diagnosed by a neurologist and evaluated by the Upper and Lower Face Apraxia Test. Buccofacial Apraxia was quantified also by a specific camera, with an appropriately developed software, able to detect the range of motion of automatic face movements and the range of the same movements on voluntary requests. In order to improve voluntary movements, the participant completed fifteen 1-hour rehabilitation sessions, composed of a 20-minutes immersive Action Observation Therapy followed by a 40-minutes Virtual Reality Augmented Feedback sessions, 5 days a week, for 3 consecutive weeks. Results: After treatment, participant achieved great improvements in quality and range of facial movements, performing most of the facial expressions (eg, kiss, smile, lateral angle of mouth displacement) without unsolicited movement. Furthermore, the Upper and Lower Face Apraxia Test showed an improvement of 118% for the Upper Face movements and of 200% for the Lower Face movements. Conclusion: Performing voluntary movement in a Virtual Reality environment with Augmented Feedbacks, in addition to Action Observation Therapy, improved performances of facial gestures and consolidate the activations by the central nervous system based on principles of experience-dependent neural plasticity.
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Many neuropsychological theories agree that the brain maintains a relatively persistent representation of one’s own body, as indicated by vivid “phantom” experiences. It remains unclear how the loss of sensory and motor information contributes to the presence of this representation. Here, we focus on new empirical and theoretical evidence of phantom sensations following damage to or an anesthetic block of the brachial plexus. We suggest a crucial role of this structure in understanding the interaction between peripheral and central mechanisms in health and in pathology. Studies of brachial plexus function have shed new light on how neuroplasticity enables “somatotopic interferences”, including pain and body awareness. Understanding the relations among clinical disorders, their neural substrate, and behavioral outcomes may enhance methods of sensory rehabilitation for phantom limbs.
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Corporeal awareness of body unity, continuity, and integrity is hardwired in the brain, even following massive deafferentation. Following peripheral limb injury, referred phantom sensations are reported frequently on the cheek and, rarely, on the ear. Here, we explore how brain plasticity mechanisms induced by multisensory stimulation of different facial regions (cheek and ear) modulate the feeling that a complete missing limb is still attached to the body. We applied the modified rubber hand illusion (RHI) paradigm following synchronous and asynchronous stimulation of the face–hand and ear–hand in the unusual case of a patient with a brachial plexus lesion, who had lost upper-left limb sensation and developed a phantom sensation of the arm restricted to the ear. He experienced a strong illusion of ownership of the rubber hand during synchronous stroking of the ear but not the cheek and reported more defined tactile sensations in his previously numb body part during the illusion than when simply touching the ear. Phantom experiences are not exclusively based on sensory memories of the once-present body periphery, they are organized into a topographic cortical map with the ear–hand area adjoining but separate from the face. Multimodal experiences specifically modulate possible remapping of ear–hand representations and generate a more defined connection between the brain’s memory of the body and what one feels of the actual physical body. We suggest that RHI is a form of sensory intervention that makes the best use of residual signals from disconnected body parts after peripheral injury, evoking and controlling the limb sensations.
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Growing evidence indicates that perceptual-motor codes may be associated with and influenced by actual bodily states. Following a spinal cord injury (SCI), for example, individuals exhibit reduced visual sensitivity to biological motion. However, a dearth of direct evidence exists about whether profound alterations in sensorimotor traffic between the body and brain influence audio-motor representations. We tested 20 wheelchair-bound individuals with lower skeletal-level SCI who were unable to feel and move their lower limbs, but have retained upper limb function. In a two-choice, matching-to-sample auditory discrimination task, the participants were asked to determine which of two action sounds matched a sample action sound presented previously. We tested aural discrimination ability using sounds that arose from wheelchair, upper limb, lower limb, and animal actions. Our results indicate that an inability to move the lower limbs did not lead to impairment in the discrimination of lower limb-related action sounds in SCI patients. Importantly, patients with SCI discriminated wheelchair sounds more quickly than individuals with comparable auditory experience (i.e. physical therapists) and inexperienced, able-bodied subjects. Audio-motor associations appear to be modified and enhanced to incorporate external salient tools that now represent extensions of their body schemas.
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Limb apraxia is a heterogeneous disorder of skilled action and tool use that has long perplexed clinicians and researchers. It occurs after damage to various loci in a densely interconnected network of regions in the left temporal, parietal, and frontal lobes. Historically, a highly classificatory approach to the study of apraxia documented numerous patterns of performance related to two major apraxia subtypes: ideational and ideomotor apraxia. More recently, there have been advances in our understanding of the functional neuroanatomy and connectivity of the left-hemisphere "tool use network," and the patterns of performance that emerge from lesions to different loci within this network. This chapter focuses on the left inferior parietal lobe, and its role in tool and body representation, action prediction, and action selection, and how these functions relate to the deficits seen in patients with apraxia subsequent to parietal lesions. Finally, suggestions are offered for several future directions that will benefit the study of apraxia, including increased attention to research on rehabilitation of this disabling disorder.
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