ArticlePDF Available

Abstract and Figures

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.
Content may be subject to copyright.
published: 03 April 2019
doi: 10.3389/fneur.2019.00309
Frontiers in Neurology | 1April 2019 | Volume 10 | Article 309
Edited by:
Giorgio Sandrini,
University of Pavia, Italy
Reviewed by:
Marianna Capecci,
Polytechnical University of Marche,
Marialuisa Gandolfi,
University of Verona, Italy
Mariella Pazzaglia
Specialty section:
This article was submitted to
a section of the journal
Frontiers in Neurology
Received: 30 August 2018
Accepted: 11 March 2019
Published: 03 April 2019
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
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.
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).
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
Frontiers in Neurology | 2April 2019 | Volume 10 | Article 309
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.
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
Frontiers in Neurology | 3April 2019 | Volume 10 | Article 309
Pazzaglia and Galli Neurorehabilitation and Apraxia
TABLE 1 | Apraxia intervention studies.
References Number of participants Treatment
Type of
Control Intervention Perceptual aspects
of training
Improvements in
experimental group
No effect
van Heugten
et al. (47)
33 30 min for 12
Strategy training Observation of picture
sequences Imagination
ADL Barthel Index
Apraxia Test Motor
Goldenberg and
Hagmann (9)
15 5 weeks Three
activities from
the domains
dressing, and
Direct training of
the activity:
completion of the
The patients perform
action immediately after
observing the
10 patients improved
on all three trained
6 months later,
improvement is
not maintained
without practice
Smania et al. (45) 6 7 35 sessions,
three per
Gesture execution
Observation of picture
(context, object)
Gesture recognition
Apraxia Test Gesture
Oral apraxia
Donkervoort et al.
42 48 8 weeks Everyday
Strategy training Observation of picture
sequences Imagination
ADL Barthel Index Apraxia Test ADL
Goldenberg et al.
6 4 weeks Four everyday
Explorative training
vs. Direct training
of the activity
The patients perform
action immediately after
observing the
Direct training of activity
reduced errors and
amount of assistance
training had no
effect on
Smania et al. (22) 18 15 30 sessions,
three per
Gesture execution
Observation of picture
(context, object)
Gesture recognition
Apraxia Test Gesture
recognition ADL
Oral apraxia
Geusgens et al.
56 57 25 sessions,
8 weeks
Action of daily
Strategy training Observation of picture
ADL untrained
Geusgens et al.
29 25 sessions,
8 weeks
Action of daily
Strategy training Observation of picture
Apraxia Test ADL
trained ADL untrained
Barthel Index
Functional Motor
Bolognini et al.
6 6 3 sessions,
10 min
Limb gesture
Anodal tDCS on
the left parietal
Imitation (observation
Imitation execution tDCS on the motor
Frontiers in Neurology | 4April 2019 | Volume 10 | Article 309
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.
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).
Frontiers in Neurology | 5April 2019 | Volume 10 | Article 309
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.
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.
MP: study concept and design, manuscript development, and
writing. GG: contributed to the writing of the manuscript.
This work was supported by the Italian Ministry of Health
(RF-2018-12365682 to MP).
Frontiers in Neurology | 6April 2019 | Volume 10 | Article 309
Pazzaglia and Galli Neurorehabilitation and Apraxia
1. Leiguarda RC, Marsden CD. Limb apraxias: higher-order disorders
of sensorimotor integration. Brain. (2000) 123(Pt 5):860–79.
doi: 10.1093/brain/123.5.860
2. Haaland KY, Harrington DL, Knight RT. Neural representations
of skilled movement. Brain. (2000) 123(Pt 11):2306–13.
doi: 10.1093/brain/123.11.2306
3. Rothi LJ, Heilman KM. Acquisition and retention of gestures by apraxic
patients. Brain Cogn. (1984) 3:426–37. doi: 10.1016/0278-2626(84)90032-0
4. Petreska B, Adriani M, Blanke O, Billard AG. Apraxia: a review. Prog Brain
Res. (2007) 164:61–83. doi: 10.1016/S0079-6123(07)64004-7
5. Wheaton LA, Hallett M. Ideomotor apraxia: a review. J Neurol Sci. (2007)
260:1–10. doi: 10.1016/j.jns.2007.04.014
6. Nobusako S, Ishibashi R, Takamura Y, Oda E, Tanigashira Y, Kouno M, et al.
Distortion of visuo-motor temporal integration in apraxia: evidence from
delayed visual feedback detection tasks and voxel-based lesion-symptom
mapping. Front Neurol. (2018) 9:709. doi: 10.3389/fneur.2018.00709
7. Foundas AL, Macauley BL, Raymer AM, Maher LM, Heilman KM,
Gonzalez Rothi LJ. Ecological implications of limb apraxia: evidence
from mealtime behavior. J Int Neuropsychol Soc. (1995) 1:62–6.
doi: 10.1017/S1355617700000114
8. Hanna-Pladdy B, Heilman KM, Foundas AL. Ecological implications
of ideomotor apraxia: evidence from physical activities of daily living.
Neurology. (2003) 60:487–90. doi: 10.1212/WNL.60.3.487
9. Goldenberg G, Hagmann J. Therapy of activities of daily living in patients
with apraxia. Neuropsychol Rehabil. (1998) 8:123–41. doi: 10.1080/713755559
10. van Heugten CM, Dekker J, Deelman BG, Stehmann-Saris JC, Kinebanian
A. Rehabilitation of stroke patients with apraxia: the role of additional
cognitive and motor impairments. Disabil Rehabil. (2000) 22:547–54.
doi: 10.1080/096382800416797
11. Sunderland A, Walker CM, Walker MF. Action errors and dressing
disability after stroke: an ecological approach to neuropsychological
assessment and intervention. Neuropsychol Rehabil. (2006) 16:666–83.
doi: 10.1080/09602010500204385
12. Borod JC, Fitzpatrick PM, Helm-Estabrooks N, Goodglass H. The
relationship between limb apraxia and the spontaneous use of
communicative gesture in aphasia. Brain Cogn. (1989) 10:121–31.
doi: 10.1016/0278-2626(89)90079-1
13. Tabaki NE, Vikelis M, Besmertis L, Vemmos K, Stathis P, Mitsikostas DD.
Apraxia related with subcortical lesions due to cerebrovascular disease. Acta
Neurol Scand. (2010) 122:9–14. doi: 10.1111/j.1600-0404.2009.01224.x
14. Saeki S, Ogata H, Okubo T, Takahashi K, Hoshuyama T. Factors
influencing return to work after stroke in Japan. Stroke. (1993) 24:1182–5.
doi: 10.1161/01.STR.24.8.1182
15. Zwinkels A, Geusgens C, van de Sande P, Van Heugten C. Assessment
of apraxia: inter-rater reliability of a new apraxia test, association
between apraxia and other cognitive deficits and prevalence of
apraxia in a rehabilitation setting. Clin Rehabil. (2004) 18:819–27.
doi: 10.1191/0269215504cr816oa
16. Hodges JR, Bozeat S, Lambon Ralph MA, Patterson K, Spatt J. The role of
conceptual knowledge in object use evidence from semantic dementia. Brain.
(2000) 123:1913–25. doi: 10.1093/brain/123.9.1913
17. Holl AK, Ille R, Wilkinson L, Otti DV, Hödl E, Herranhof B, et al. Impaired
ideomotor limb apraxia in cortical and subcortical dementia: a comparison
of Alzheimer’s and Huntington’s disease. Neurodegener Dis. (2011) 8:208–15.
doi: 10.1159/000322230
18. Nelissen N, Pazzaglia M, Vandenbulcke M, Sunaert S, Fannes K, Dupont P,
et al. Gesture discrimination in primary progressive aphasia: the intersection
between gesture and language processing pathways. J Neurosci. (2010)
30:6334–41. doi: 10.1523/JNEUROSCI.0321-10.2010
19. Cantagallo A, Maini M, Rumiati RI. The cognitive rehabilitation of limb
apraxia in patients with stroke. Neuropsychol Rehabil. (2012) 22:473–88.
doi: 10.1080/09602011.2012.658317
20. Worthington A. Treatments and technologies in the rehabilitation of apraxia
and action disorganisation syndrome: a review. Neurorehabilitation. (2016)
39:163–74. doi: 10.3233/NRE-161348
21. French B, Thomas LH, Coupe J, McMahon NE, Connell L, Harrison
J, et al. Repetitive task training for improving functional ability
after stroke. Cochrane Database Syst Rev. (2007) 11:CD006073.
doi: 10.1002/14651858.CD006073.pub2
22. Smania N, Aglioti SM, Girardi F, Tinazzi M, Fiaschi A, Cosentino
A, et al. Rehabilitation of limb apraxia improves daily life
activities in patients with stroke. Neurology. (2006) 67:2050–2.
doi: 10.1212/01.wnl.0000247279.63483.1f
23. Buxbaum LJ, Haaland KY, Hallett M, Wheaton L, Heilman KM, Rodriguez
A, et al. Treatment of limb apraxia: moving forward to improved action. Am
J Phys Med Rehabil. (2008) 87:149–61. doi: 10.1097/PHM.0b013e31815e6727
24. Etcharry-Bouyx F, Le Gall D, Jarry C, Osiurak F. Gestural apraxia. Rev Neurol.
(2017) 173:430–9. doi: 10.1016/j.neurol.2017.07.005
25. Wang L, Goodglass H. Pantomime, praxis, and aphasia. Brain Lang. (1992)
42:402–18. doi: 10.1016/0093-934X(92)90076-Q
26. Goldenberg G. Matching and imitation of hand and finger postures in
patients with damage in the left or right hemispheres. Neuropsychologia.
(1999) 37:559–66. doi: 10.1016/S0028-3932(98)00111-0
27. Hommel B, Musseler J, Aschersleben G, Prinz W. The Theory of Event
Coding (TEC): a framework for perception and action planning. Behav Brain
Sci. (2001) 24:849–78. doi: 10.1017/S0140525X01000103
28. Schutz-Bosbach S, Prinz W. Perceptual resonance: action-induced
modulation of perception. Trends Cogn Sci. (2007) 11:349–55.
doi: 10.1016/j.tics.2007.06.005
29. Sunderland A, Sluman SM. Ideomotor apraxia, visuomotor control and
the explicit representation of posture. Neuropsychologia. (2000) 38:923–34.
doi: 10.1016/S0028-3932(00)00021-X
30. Pazzaglia M, Smania N, Corato E, Aglioti SM. Neural underpinnings of
gesture discrimination in patients with limb apraxia. J Neurosci. (2008)
28:3030–41. doi: 10.1523/JNEUROSCI.5748-07.2008
31. Heilman KM, Rothi LJ, Valenstein E. Two forms of ideomotor apraxia.
Neurology. (1982) 32:342–6. doi: 10.1212/WNL.32.4.342
32. Kalenine S, Buxbaum LJ, Coslett HB. Critical brain regions for action
recognition: lesion symptom mapping in left hemisphere stroke. Brain.
(2010) 133:3269–80. doi: 10.1093/brain/awq210
33. Rothi LJ, Heilman KM, Watson RT. Pantomime comprehension and
ideomotor apraxia. J Neurol Neurosurg Psychiatry. (1985) 48:207–10.
doi: 10.1136/jnnp.48.3.207
34. Weiss PH, Rahbari NN, Hesse MD, Fink GR. Deficient
sequencing of pantomimes in apraxia. Neurology. (2008) 70:834–40.
doi: 10.1212/01.wnl.0000297513.78593.dc
35. Pazzaglia M, Pizzamiglio L, Pes E, Aglioti SM. The sound of actions in
apraxia. Curr Biol. (2008) 18:1766–72. doi: 10.1016/j.cub.2008.09.061
36. Mutha PK, Stapp LH, Sainburg RL, Haaland KY. Motor adaptation
deficits in ideomotor apraxia. J Int Neuropsychol Soc. (2017) 23:139–49.
doi: 10.1017/S135561771600120X
37. Fontana AP, Kilner JM, Rodrigues EC, Joffily M, Nighoghossian N, Vargas
CD, et al. Role of the parietal cortex in predicting incoming actions.
NeuroImage. (2012) 59:556–64. doi: 10.1016/j.neuroimage.2011.07.046
38. Pazzaglia M. Does what you hear predict what you will do and say? Behav
Brain Sci. (2013) 36:370–1. doi: 10.1017/S0140525X12002804
39. Pazzaglia M. Impact commentaries. Action discrimination: impact
of apraxia. J Neurol Neurosurg Psychiatry. (2013) 84:477–8.
doi: 10.1136/jnnp-2012-304817
40. Buxbaum LJ, Randerath J. Limb apraxia and the left parietal lobe. Handb Clin
Neurol. (2018) 151:349–63. doi: 10.1016/B978-0-444-63622-5.00017-6
41. Pazzaglia M, Galli G. Translating novel findings of perceptual-motor codes
into the neuro-rehabilitation of movement disorders. Front Behav Neurosci.
9:222. doi: 10.3389/fnbeh.2015.00222
42. Garrison KA, Winstein CJ, Aziz-Zadeh L. The mirror neuron system: a
neural substrate for methods in stroke rehabilitation. Neurorehabil Neural
Repair. (2010) 24:404–12. doi: 10.1177/1545968309354536
43. Small SL, Buccino G, Solodkin A. The mirror neuron system and treatment
of stroke. Dev Psychobiol. (2012) 54:293–310. doi: 10.1002/dev.20504
44. Bartolo A, Cubelli R, Della Sala S. Cognitive approach to the
assessment of limb apraxia. Clin Neuropsychol. (2008) 22:27–45.
doi: 10.1080/13854040601139310
Frontiers in Neurology | 7April 2019 | Volume 10 | Article 309
Pazzaglia and Galli Neurorehabilitation and Apraxia
45. Smania N, Girardi F, Domenicali C, Lora E, Aglioti S. The rehabilitation of
limb apraxia: a study in left-brain-damaged patients. Arch Phys Med Rehabil.
(2000) 81:379–88. doi: 10.1053/mr.2000.6921
46. Goldenberg G, Daumuller M, Hagmann S. Assessment and therapy of
complex activities of daily living in apraxia. Neuropsychol Rehabil. (2001)
11:147–69. doi: 10.1080/09602010042000204
47. van Heugten CM, Dekker J, Deelman BG, van Dijk AJ, Stehmann-
Saris JC, Kinebanian A. Outcome of strategy training in stroke patients
with apraxia: a phase II study. Clin Rehabil. (1998) 12:294–303.
doi: 10.1191/026921598674468328
48. Donkervoort M, Dekker J, Stehmann-Saris FC, Deeolman BG. Efficacy
of strategy training in left hemisphere stroke patients with apraxia:
a randomised clinical trial. Neuropsychol Rehabil. (2001) 11:549–66.
doi: 10.1080/09602010143000093
49. Geusgens CA, van Heugten CM, Cooijmans JP, Jolles J, van den
Heuvel WJ. Transfer effects of a cognitive strategy training for stroke
patients with apraxia. J Clin Exp Neuropsychol. (2007) 29:831–41.
doi: 10.1080/13803390601125971
50. Geusgens C, van Heugten C, Donkervoort M, van den Ende E, Jolles J,
van den Heuvel W. Transfer of training effects in stroke patients with
apraxia: an exploratory study. Neuropsychol Rehabil. (2006) 16:213–29.
doi: 10.1080/09602010500172350
51. Bolognini N, Convento S, Banco E, Mattioli F, Tesio L, Vallar G. Improving
ideomotor limb apraxia by electrical stimulation of the left posterior parietal
cortex. Brain. (2015) 138:428–39. doi: 10.1093/brain/awu343
52. Buccino G. Action observation treatment: a novel tool in neurorehabilitation.
Philos Trans R Soc Lond Ser B Biol Sci. (2014) 369:20130185.
doi: 10.1098/rstb.2013.0185
53. Oouchida Y, Suzuki E, Aizu N, Takeuchi N, Izumi SI. Applications of
observational learning in neurorehabilitation. Int J Phys Med Rehabil. (2013)
1:146. doi: 10.4172/2329-9096.1000146
54. Rothi LJ, Heilman KM. Apraxia, the Neuropsychology of Action. Hove:
Psychology Press (1997).
55. Pazzaglia M, Galli G. Loss of agency in apraxia. Front Hum Neurosci. (2014)
8:751. doi: 10.3389/fnhum.2014.00751
56. Badets A, Blandin Y, Wright DL, Shea CH. Error detection processes
during observational learning. Res Q Exerc Sport. (2006) 77:177–84.
doi: 10.1080/02701367.2006.10599352
57. Badets A, Blandin Y, Shea CH. Intention in motor learning
through observation. Q J Exp Psychol. (2006) 59:377–86.
doi: 10.1080/02724980443000773
58. Heyes CM, Foster CL. Motor learning by observation: evidence from
a serial reaction time task. Q J Exp Psychol. (2002) 55:593–607.
doi: 10.1080/02724980143000389
59. Buchanan JJ, Dean NJ. Specificity in practice benefits learning in novice
models and variability in demonstration benefits observational practice.
Psychol Res. (2010) 74:313–26. doi: 10.1007/s00426-009-0254-y
60. Hecht H, Vogt S, Prinz W. Motor learning enhances perceptual judgment:
a case for action-perception transfer. Psychol Res. (2001) 65:3–14.
doi: 10.1007/s004260000043
61. Casile A, Giese MA. Nonvisual motor training influences biological motion
perception. Curr Biol. (2006) 16:69–74. doi: 10.1016/j.cub.2005.10.071
62. Rosenkranz K, Williamon A, Rothwell JC. Motorcortical excitability and
synaptic plasticity is enhanced in professional musicians. J Neurosci. (2007)
27:5200–6. doi: 10.1523/JNEUROSCI.0836-07.2007
63. Kleim JA, Hogg TM, VandenBerg PM, Cooper NR, Bruneau R, Remple M.
Cortical synaptogenesis and motor map reorganization occur during late,
but not early, phase of motor skill learning. J Neurosci. (2004) 24:628–33.
doi: 10.1523/JNEUROSCI.3440-03.2004
64. Sale P, Franceschini M. Action observation and mirror neuron network: a
tool for motor stroke rehabilitation. Eur J Phys Rehabil Med. (2012) 48:313–8.
65. Franceschini M, Ceravolo MG, Agosti M, Cavallini P, Bonassi S, Dall’Armi
V, et al. Clinical relevance of action observation in upper-limb stroke
rehabilitation: a possible role in recovery of functional dexterity. A
randomized clinical trial. Neurorehabil Neural Repair. (2012) 26:456–62.
doi: 10.1177/1545968311427406
66. Sale P, Ceravolo MG, Franceschini M. Action observation therapy in the
subacute phase promotes dexterity recovery in right-hemisphere stroke
patients. Biomed Res Int. (2014) 2014:457538. doi: 10.1155/2014/457538
67. Park HR, Kim JM, Lee MK, Oh DW. Clinical feasibility of action
observation training for walking function of patients with post-stroke
hemiparesis: a randomized controlled trial. Clin Rehabil. (2014) 28:794–803.
doi: 10.1177/0269215514523145
68. Bang DH, Shin WS, Kim SY, Choi JD. The effects of action observational
training on walking ability in chronic stroke patients: a double-
blind randomized controlled trial. Clin Rehabil. (2013) 27:1118–25.
doi: 10.1177/0269215513501528
69. Kim SS, Kim TH, Lee BH. Effects of action observational training on cerebral
hemodynamic changes of stroke survivors: a fTCD study. J Phys Ther Sci.
(2014) 26:331–4. doi: 10.1589/jpts.26.331
70. Bonifazi S, Tomaiuolo F, Altoè G, Ceravolo MG, Provinciali L, Marangolo
P. Action observation as a useful approach for enhancing recovery of
verb production: new evidence from aphasia. Eur J Phys Rehabil Med.
(2013) 49:473–81.
71. Marangon M, Priftis K, Fedeli M, Masiero S, Tonin P, Piccione F.
Lateralization of motor cortex excitability in stroke patients during
action observation: a TMS study. Biomed Res. Int. (2014) 2014:251041.
doi: 10.1155/2014/251041
72. Brunner IC, Skouen JS, Ersland L, Gruner R. Plasticity and response to
action observation: a longitudinal FMRI study of potential mirror neurons in
patients with subacute stroke. Neurorehabil Neural Repair. (2014) 28:874–84.
doi: 10.1177/1545968314527350
73. Ertelt D, Binkofski F. Action observation as a tool for neurorehabilitation to
moderate motor deficits and aphasia following stroke. Neural Regener Res.
(2012) 7:2063–74. doi: 10.3969/j.issn.1673-5374.2012.26.008
74. Ertelt D, Hemmelmann C, Dettmers C, Ziegler A, Binkofski F. Observation
and execution of upper-limb movements as a tool for rehabilitation of motor
deficits in paretic stroke patients: protocol of a randomized clinical trial.
BMC Neurol. (2012) 12:42. doi: 10.1186/1471-2377-12-42
75. Ertelt D, Small S, Solodkin A, Dettmers C, McNamara A, Binkofski
F, et al. Action observation has a positive impact on rehabilitation of
motor deficits after stroke. Neuroimage. (2007) 36(Suppl. 2):T164–73.
doi: 10.1016/j.neuroimage.2007.03.043
76. Franceschini M, Agosti M, Cantagallo A, Sale P, Mancuso M, Buccino
G. Mirror neurons: action observation treatment as a tool in stroke
rehabilitation. Eur J Phys Rehabil Med. (2010) 46:517–23.
77. Kim E, Kim K. Effect of purposeful action observation on upper
extremity function in stroke patients. J Phys Ther Sci. (2015) 27:2867–9.
doi: 10.1589/jpts.27.2867
78. Harmsen WJ, Bussmann JB, Selles RW, Hurkmans HL, Ribbers GM.
A mirror therapy-based action observation protocol to improve motor
learning after stroke. Neurorehabil Neural Repair. (2015) 29:509–16.
doi: 10.1177/1545968314558598
79. Dettmers C, Nedelko V, Hassa T, Starrost K, Schoenfeld MA. “Video
Therapy”: promoting hand function after stroke by action observation
training – a pilot randomized controlled trial. Int J Phys Med Rehabil. (2014)
2:189. doi: 10.4172/2329-9096.1000189
80. Zhu M-H, Wang J, Gu X-D, Shi M-F, Zeng M, Wang C-Y, et al. Effect of
action observation therapy on daily activities and motor recovery in stroke
patients. Int J Nurs Sci. (2015) 2:279–82. doi: 10.1016/j.ijnss.2015.08.006
81. Kim C, Bang D. Action observation training enhances upper extremity
function in subacute stroke survivor with moderate impairment: a double-
blind, randomized controlled pilot trial. J Korean Soc Phys Med. (2016)
11:133–40. doi: 10.13066/kspm.2016.11.1.133
82. Kuk EJ, Kim JM, Oh DW, Hwang HJ. Effects of action observation
therapy on hand dexterity and EEG-based cortical activation patterns in
patients with post-stroke hemiparesis. Top Stroke Rehabil. (2016) 23:318–25.
doi: 10.1080/10749357.2016.1157972
83. Fu J, Zeng M, Shen F, Cui Y, Zhu M, Gu X, et al. Effects of action
observation therapy on upper extremity function, daily activities and motion
evoked potential in cerebral infarction patients. Medicine. (2017) 96:e8080.
doi: 10.1097/MD.0000000000008080
Frontiers in Neurology | 8April 2019 | Volume 10 | Article 309
Pazzaglia and Galli Neurorehabilitation and Apraxia
84. Celnik P, Webster B, Glasser DM, Cohen LG. Effects of action
observation on physical training after stroke. Stroke. (2008) 39:1814–20.
doi: 10.1161/STROKEAHA.107.508184
85. Cowles T, Clark A, Mares K, Peryer G, Stuck R, Pomeroy V. Observation-
to-imitate plus practice could add little to physical therapy benefits within 31
days of stroke: translational randomized controlled trial. Neurorehabil Neural
Repair. (2013) 27:173–82. doi: 10.1177/1545968312452470
86. Lee D, Roh H, Park J, Lee S, Han S. Drinking behavior training for stroke
patients using action observation and practice of upper limb function. J Phys
Ther Sci. (2013) 25:611–4. doi: 10.1589/jpts.25.611
87. Pelosin E, Bove M, Ruggeri P, Avanzino L, Abbruzzese G. Reduction of
bradykinesia of finger movements by a single session of action observation
in Parkinson disease. Neurorehabil Neural Repair. (2013) 27:552–60.
doi: 10.1177/1545968312471905
88. Buccino G, Gatti R, Giusti MC, Negrotti A, Rossi A, Calzetti S, et al. Action
observation treatment improves autonomy in daily activities in Parkinson’s
disease patients: results from a pilot study. Mov Disord. (2011) 26:1963–4.
doi: 10.1002/mds.23745
89. Esculier JF, Vaudrin J, Tremblay LE. Corticomotor excitability in Parkinson’s
disease during observation, imagery and imitation of action: effects of
rehabilitation using wii fit and comparison to healthy controls. J Parkinson’s
Dis. (2014) 4:67–75. doi: 10.3233/JPD-130212
90. Pelosin E, Avanzino L, Bove M, Stramesi P, Nieuwboer A, Abbruzzese
G. Action observation improves freezing of gait in patients with
Parkinson’s disease. Neurorehabil Neural Repair. (2010) 24:746–52.
doi: 10.1177/1545968310368685
91. Castiello U, Ansuini C, Bulgheroni M, Scaravilli T, Nicoletti R. Visuomotor
priming effects in Parkinson’s disease patients depend on the match between
the observed and the executed action. Neuropsychologia. (2009) 47:835–42.
doi: 10.1016/j.neuropsychologia.2008.12.016
92. Tremblay F, Leonard G, Tremblay L. Corticomotor facilitation associated
with observation and imagery of hand actions is impaired in Parkinson’s
disease. Exp Brain Res. (2008) 185:249–57. doi: 10.1007/s00221-007-1150-6
93. Sgandurra G, Ferrari A, Cossu G, Guzzetta A, Fogassi L, Cioni G.
Randomized trial of observation and execution of upper extremity actions
versus action alone in children with unilateral cerebral palsy. Neurorehabil
Neural Repair. (2013) 27:808–15. doi: 10.1177/1545968313497101
94. Sgandurra G, Ferrari A, Cossu G, Guzzetta A, Biagi L, Tosetti M, et al.
Upper limb children action-observation training (UP-CAT): a randomised
controlled trial in hemiplegic cerebral palsy. BMC Neurol. (2011) 11:80.
doi: 10.1186/1471-2377-11-80
95. Buccino G, Arisi D, Gough P, Aprile D, Ferri C, Serotti L, et al. Improving
upper limb motor functions through action observation treatment: a pilot
study in children with cerebral palsy. Dev Med Child Neurol. (2012) 54:822–8.
doi: 10.1111/j.1469-8749.2012.04334.x
96. Kim JY, Kim JM, Ko EY. The effect of the action obser vation physical training
on the upper extremity function in children with cerebral palsy. J Exerc
Rehabil. (2014) 10:176–83. doi: 10.12965/jer.140114
97. Kim JH, Lee BH. Action observation training for functional activities
after stroke: a pilot randomized controlled trial. Neurorehabilitation. (2013)
33:565–74. doi: 10.3233/NRE-130991
98. Celnik P, Stefan K, Hummel F, Duque J, Classen J, Cohen LG. Encoding a
motor memory in the older adult by action observation. Neuroimage. (2006)
29:677–84. doi: 10.1016/j.neuroimage.2005.07.039
99. Liepert J, Greiner J, Dettmers C. Motor excitability changes during
action observation in stroke patients. J Rehabil Med. (2014) 46:400–5.
doi: 10.2340/16501977-1276
100. Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G. Parietal
lobe: from action organization to intention understanding. Science. (2005)
308:662–7. doi: 10.1126/science.1106138
101. Gallese V, Fadiga L, Fogassi L, Rizzolatti G. Action recognition
in the premotor cortex. Brain. (1996) 119 (Pt 2):593–609.
doi: 10.1093/brain/119.2.593
102. Rizzolatti G, Craighero L. The mirror-neuron system. Ann Rev Neurosci.
(2004) 27:169–92. doi: 10.1146/annurev.neuro.27.070203.144230
103. Kilner JM. More than one pathway to action understanding. Trends Cogn Sci.
(2011) 15:352–7. doi: 10.1016/j.tics.2011.06.005
104. Hermsdorfer J, Li Y, Randerath J, Roby-Brami A, Goldenberg G. Tool
use kinematics across different modes of execution. Implications
for action representation and apraxia. Cortex. (2013) 49:184–99.
doi: 10.1016/j.cortex.2011.10.010
105. Leiguarda RC, Merello M, Nouzeilles MI, Balej J, Rivero A, Nogués M. Limb-
kinetic apraxia in corticobasal degeneration: clinical and kinematic features.
Mov Disord. (2003) 18:49–59. doi: 10.1002/mds.10303
106. Sirigu A, Cohen L, Duhamel JR, Pillon B, Dubois B, Agid Y. A selective
impairment of hand posture for object utilization in apraxia. Cortex. (1995)
31:41–55. doi: 10.1016/S0010-9452(13)80104-9
107. Sirigu A, Duhamel JR, Cohen L, Pillon B, Dubois B, Agid Y. The
mental representation of hand movements after parietal cortex
damage. Science. (1996) 273:1564–8. doi: 10.1126/science.273.
108. Grezes J, Decety J. Functional anatomy of execution,
mental simulation, observation, and verb generation of
actions: a meta-analysis. Hum Brain Mapp. (2001) 12:1–19.
doi: 10.1002/1097-0193(200101)12:1<1::AID-HBM10>3.0.CO;2-V
109. Grafton ST. Embodied cognition and the simulation of action
to understand others. Ann N Y Acad Sci. (2009) 1156:97–117.
doi: 10.1111/j.1749-6632.2009.04425.x
110. Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti
G. Cortical mechanisms of human imitation. Science. (1999) 286:2526–8.
doi: 10.1126/science.286.5449.2526
111. Flanagan JR, Johansson RS. Action plans used in action observation. Nature.
(2003) 424:769–71. doi: 10.1038/nature01861
112. Buccino G, Binkofski F, Riggio L. The mirror neuron
system and action recognition. Brain Lang. (2004) 89:370–6.
doi: 10.1016/S0093-934X(03)00356-0
113. Buxbaum LJ, Shapiro AD, Coslett HB. Critical brain regions for tool-related
and imitative actions: a componential analysis. Brain. (2014) 137:1971–85.
doi: 10.1093/brain/awu111
114. Goldenberg G, Hermsdorfer J, Glindemann R, Rorden C, Karnath HO.
Pantomime of tool use depends on integrity of left inferior frontal cortex.
Cereb Cortex. (2007) 17:2769–76. doi: 10.1093/cercor/bhm004
115. Mengotti P, Corradi-Dell’Acqua C, Negri GA, Ukmar M, Pesavento V,
Rumiati RI. Selective imitation impairments differentially interact with
language processing. Brain. (2013). 136:2602–18. doi: 10.1093/brain/awt194
116. Weiss PH, Ubben SD, Kaesberg S, Kalbe E, Kessler J, Liebig T, et al.
Where language meets meaningful action: a combined behavior and lesion
analysis of aphasia and apraxia. Brain Struct Funct. (2016) 221:563–76.
doi: 10.1007/s00429-014-0925-3
117. Hoeren M, Kümmerer D, Bormann T, Beume L, Ludwig VM, Vry MS, et al.
Neural bases of imitation and pantomime in acute stroke patients: distinct
streams for praxis. Brain. (2014) 137:2796–810. doi: 10.1093/brain/awu203
118. De Renzi E, Lucchelli F. Ideational apraxia. Brain. (1988) 111(Pt 5):1173–85.
doi: 10.1093/brain/111.5.1173
119. Bizzozero I, Costato D, Sala SD, Papagno C, Spinnler H, Venneri A. Upper
and lower face apraxia: role of the right hemisphere. Brain. (2000) 123(Pt
11):2213–30. doi: 10.1093/brain/123.11.2213
120. Rothi LJ, Mack L, Heilman KM. Pantomime agnosia. J Neurol Neurosurg
Psychiatry. (1986) 49:451–4. doi: 10.1136/jnnp.49.4.451
121. Cubelli R, Marchetti C, Boscolo G, Della Sala S. Cognition in action:
testing a model of limb apraxia. Brain Cogn. (2000) 44:144–65.
doi: 10.1006/brcg.2000.1226
122. Bartolo A, Cubelli R, Della Sala S, Drei S, Marchetti C. Double dissociation
between meaningful and meaningless gesture reproduction in apraxia.
Cortex. (2001) 37:696–9. doi: 10.1016/S0010-9452(08)70617-8
123. Negri GA, Rumiati RI, Zadini A, Ukmar M, Mahon BZ, Caramazza A.
What is the role of motor simulation in action and object recognition?
Evidence from apraxia. Cogn Neuropsychol. (2007) 24:795–816.
doi: 10.1080/02643290701707412
124. Aglioti SM, Pazzaglia M. Representing actions through their sound. Exp
Brain Res. (2010) 206:141–51. doi: 10.1007/s00221-010-2344-x
125. Mahon BZ, Caramazza A. The orchestration of the sensory-motor
systems: clues from neuropsychology. Cogn Neuropsychol. (2005) 22:480–94.
doi: 10.1080/02643290442000446
Frontiers in Neurology | 9April 2019 | Volume 10 | Article 309
Pazzaglia and Galli Neurorehabilitation and Apraxia
126. Buxbaum LJ, Kalenine S. Action knowledge, visuomotor activation, and
embodiment in the two action systems. Ann N Y Acad Sci. (2010) 1191:201–
18. doi: 10.1111/j.1749-6632.2010.05447.x
127. Binkofski F, Buxbaum LJ. Two action systems in the human brain. Brain
Lang. (2013) 127:222–9. doi: 10.1016/j.bandl.2012.07.007
128. Pazzaglia M, Zantedeschi M. Plasticity and awareness of bodily distortion.
Neural Plast. (2016) 2016:9834340. doi: 10.1155/2016/9834340
129. Buccino G, Molinaro A, Ambrosi C, Arisi D, Mascaro L, Pinardi
C, et al. Action observation treatment improves upper limb motor
functions in children with cerebral palsy: a combined clinical and brain
imaging study. Neural Plast. (2018) 2018:4843985. doi: 10.1155/2018/
130. Hanna-Pladdy B, Heilman KM, Foundas AL. Cortical and subcortical
contributions to ideomotor apraxia: analysis of task demands and error
types. Brain. (2001) 124:2513–27. doi: 10.1093/brain/124.12.2513
131. Moro V, Urgesi C, Pernigo S, Lanteri P, Pazzaglia M, Aglioti SM. The neural
basis of body form and body action agnosia. Neuron. (2008) 60:235–46.
doi: 10.1016/j.neuron.2008.09.022
132. Halsband U, Schmitt J, Weyers M, Binkofski F, Grützner G, Freund HJ.
Recognition and imitation of pantomimed motor acts after unilateral parietal
and premotor lesions: a perspective on apraxia. Neuropsychologia. (2001)
39:200–16. doi: 10.1016/S0028-3932(00)00088-9
133. Hickok G. Eight problems for the mirror neuron theory of action
understanding in monkeys and humans. J Cogn Neurosci. (2009) 21:1229–43.
doi: 10.1162/jocn.2009.21189
134. Fogassi L, Luppino G. Motor functions of the parietal lobe. Curr Opin
Neurobiol. (2005) 15:626–31. doi: 10.1016/j.conb.2005.10.015
135. Stefan K, Cohen LG, Duque J, Mazzocchio R, Celnik P, Sawaki L, et al.
Formation of a motor memory by action observation. J Neurosci. (2005)
25:9339–46. doi: 10.1523/JNEUROSCI.2282-05.2005
136. Bianchi M, Cosseddu M, Cotelli M, Manenti R, Brambilla M, Rizzetti MC,
et al. Left parietal cortex transcranial direct current stimulation enhances
gesture processing in corticobasal syndrome. Eur J Neurol. (2015) 22:1317–
22. doi: 10.1111/ene.12748
137. Baldwin KA, McCoy SL. Making a case for acute ischemic stroke. J Pharm
Pract. (2010) 23:387–97. doi: 10.1177/0897190010372325
138. Ferro JM, Martins IP, Mariano G, Caldas AC. CT scan correlates of
gesture recognition. J Neurol Neurosurg Psychiatry. (1983) 46:943–52.
doi: 10.1136/jnnp.46.10.943
139. Catmur C, Gillmeister H, Bird G, Liepelt R, Brass M, Heyes C.
Through the looking glass: counter-mirror activation following
incompatible sensorimotor learning. Eur J Neurosci. (2008) 28:1208–15.
doi: 10.1111/j.1460-9568.2008.06419.x
140. Gazzola V, Rizzolatti G, Wicker B, Keysers C. The anthropomorphic
brain: the mirror neuron system responds to human and robotic actions.
Neuroimage. (2007) 35:1674–84. doi: 10.1016/j.neuroimage.2007.02.003
141. Mattar AA, Gribble PL. Motor learning by observing. Neuron. (2005)
46:153–60. doi: 10.1016/j.neuron.2005.02.009
142. Buccino G, Solodkin A, Small SL. Functions of the mirror neuron system:
implications for neurorehabilitation. Cogn Behav Neurol. (2006) 19:55–63.
doi: 10.1097/00146965-200603000-00007
143. Dinstein I, Gardner JL, Jazayeri M, Heeger DJ. Executed and observed
movements have different distributed representations in human aIPS. J
Neurosci. (2008) 28:11231–9. doi: 10.1523/JNEUROSCI.3585-08.2008
144. Mahon BZ. Action recognition: is it a motor process? Curr Biol. (2008)
18:R1068–9. doi: 10.1016/j.cub.2008.10.001
145. Tkach D, Reimer J, Hatsopoulos NG. Congruent activity during action
and action observation in motor cortex. J Neurosci. (2007) 27:13241–50.
doi: 10.1523/JNEUROSCI.2895-07.2007
146. Brown LE, Wilson ET, Gribble PL. Repetitive transcranial magnetic
stimulation to the primary motor cortex interferes with motor learning by
observing. J Cogn Neurosci. (2009) 21:1013–22. doi: 10.1162/jocn.2009.21079
147. Pazzaglia M, Galli G, Lewis JW, Scivoletto G, Giannini AM, Molinari M.
Embodying functionally relevant action sounds in patients with spinal cord
injury. Sci Rep. (2018) 8:15641. doi: 10.1038/s41598-018-34133-z
148. Pazzaglia M. Body and odors: not just molecules, after all. Curr Dir Psychol
Sci. (2015) 24:329–33. doi: 10.1177/0963721415575329
149. Aglioti SM, Pazzaglia M. Sounds and scents in (social) action. Trends Cogn
Sci. (2011) 15:47–55. doi: 10.1016/j.tics.2010.12.003
150. Pazzaglia M, Galli G, Lucci G, Scivoletto G, Molinari M, Haggard P. Phantom
limb sensations in the ear of a patient with a brachial plexus lesion. Cortex.
(2018). doi: 10.1016/j.cortex.2018.08.020. [Epub ahead of print].
151. Pazzaglia M, Haggard P, Scivoletto G, Molinari M, Lenggenhager B. Pain and
somatic sensation are transiently normalized by illusory body ownership in
a patient with spinal cord injury. Restor Neurol Neurosci. (2016) 34:603–13.
doi: 10.3233/RNN-150611
152. Costantini M, Bueti D, Pazzaglia M, Aglioti SM. Temporal dynamics of
visuo-tactile extinction within and between hemispaces. Neuropsychology.
(2007) 21:242–50. doi: 10.1037/0894-4105.21.2.242
153. Goldenberg G, Hentze S, Hermsdorfer J. The effect of tactile feedback
on pantomime of tool use in apraxia. Neurology. (2004) 63:1863–7.
doi: 10.1212/01.WNL.0000144283.38174.07
154. Pazzaglia M, Leemhuis E, Giannini AM, Haggard P. The Homuncular Jigsaw:
investigations of phantom limb and body awareness following brachial
plexus block or avulsion. J Clin Med. (2019) 8:E182. doi: 10.3390/jcm8020182
155. Pazzaglia M, Scivoletto G, Giannini AM, Leemhuis E. My hand in my
ear: a phantom limb re-induced by the illusion of body ownership in
a patient with a brachial plexus lesion. Psychol Res. (2019) 83:196–204.
doi: 10.1007/s00426-018-1121-5
156. Galli G, Pazzaglia M. Commentary on: “the body social: an enactive approach
to the self ”. A tool for merging bodily and social self in immobile individuals.
Front Psychol. 6:305. doi: 10.3389/fpsyg.2015.00305
157. Lucci G, Pazzaglia M. Towards multiple interactions of inner and outer
sensations in corporeal awareness. Front Hum Neurosci. (2015) 9:163.
doi: 10.3389/fnhum.2015.00163
158. Cramer SC, Sur M, Dobkin BH, O’Brien C, Sanger TD, Trojanowski JQ,
et al. Harnessing neuroplasticity for clinical applications. Brain. (2011)
134:1591–609. doi: 10.1093/brain/awr039
159. Law LLF, Fong KNK, Li RKF. Multisensory stimulation to promote upper
extremity motor recovery in stroke: a pilot study. Brit J Occup Ther. (2018)
81:641–8. doi: 10.1177/0308022618770141
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
in this journal is cited, in accordance with accepted academic practice. No use,
distribution or reproduction is permitted which does not comply with these terms.
Frontiers in Neurology | 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]. ...
Full-text available
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. ...
Full-text available
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). ...
Full-text available
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]. ...
Full-text available
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]. ...
Full-text available
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]. ...
Full-text available
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]. ...
Full-text available
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). ...
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. ...
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. ...
Full-text available
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.
Full-text available
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.
Full-text available
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.
Full-text available
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.
Full-text available
Limb apraxia is a higher brain dysfunction that typically occurs after left hemispheric stroke and its cause cannot be explained by sensory disturbance or motor paralysis. The comparison of motor signals and visual feedback to generate errors, i.e., visuo-motor integration, is important in motor control and motor learning, which may be impaired in apraxia. However, in apraxia after stroke, it is unknown whether there is a specific deficit in visuo-motor temporal integration compared to visuo-tactile and visuo-proprioceptive temporal integration. We examined the precision of visuo-motor temporal integration and sensory-sensory (visuo-tactile and visuo-proprioception) temporal integration in apraxia after stroke by using a delayed visual feedback detection task with three different conditions (tactile, passive movement, and active movement). The delay detection threshold and the probability curve for delay detection obtained in this task were quantitative indicators of the respective temporal integration functions. In addition, we performed subtraction and voxel-based lesion-symptom mapping to identify the brain lesions responsible for apraxia and deficits in visuo-motor temporal integration. The behavioral experiments showed that the delay detection threshold was extended and that the probability curve for delay detection was less steep in apraxic patients compared to controls (pseudo-apraxic patients and unaffected patients), only for the active movement condition, and not for the tactile and passive movement conditions. Furthermore, the severity of apraxia was significantly correlated with the delay detection threshold and the steepness of the probability curve in the active movement condition. These results indicated that multisensory (i.e., visual, tactile, and proprioception) feedback was normally temporally integrated, but motor prediction and visual feedback were not correctly temporally integrated in apraxic patients. That is, apraxic patients had difficulties with visuo-motor temporal integration. Lesion analyses revealed that both apraxia and the distortion of visuo-motor temporal integration were associated with lesions in the fronto-parietal motor network, including the left inferior parietal lobule and left inferior frontal gyrus. We suppose that damage to the left inferior fronto-parietal network could cause deficits in motor prediction for visuo-motor temporal integration, but not for sensory-sensory (visuo-tactile and visuo-proprioception) temporal integration, leading to the distortion of visuo-motor temporal integration in patients with apraxia.
Full-text available
The aim of the present study was to assess the role of action observation treatment (AOT) in the rehabilitation of upper limb motor functions in children with cerebral palsy. We carried out a two-group, parallel randomized controlled trial. Eighteen children (aged 5–11 yr) entered the study: 11 were treated children, and 7 served as controls. Outcome measures were scores on two functional scales: Melbourne Assessment of Unilateral Upper Limb Function Scale (MUUL) and the Assisting Hand Assessment (AHA). We collected functional scores before treatment (T1), at the end of treatment (T2), and at two months of follow-up (T3). As compared to controls, treated children improved significantly in both scales at T2 and this improvement persisted at T3. AOT has therefore the potential to become a routine rehabilitation practice in children with CP. Twelve out of 18 enrolled children also underwent a functional magnetic resonance study at T1 and T2. As compared to controls, at T2, treated children showed stronger activation in a parieto-premotor circuit for hand-object interactions. These findings support the notion that AOT contributes to reorganize brain circuits subserving the impaired function rather than activating supplementary or vicariating ones.
Full-text available
Background: The aim of this study was to explore the effects of action observation therapy on motor function of upper extremity, activities of daily living, and motion evoked potential in cerebral infarction patients. Method: Cerebral infarction survivors were randomly assigned to an experimental group (28 patients) or a control group (25 patients). The conventional rehabilitation treatments were applied in both groups, but the experimental group received an additional action observation therapy for 8 weeks (6 times per week, 20 minutes per time). Fugl-Meyer assessment (FMA), Wolf Motor Function Test (WMFT), Modified Barthel Index (MBI), and motor evoked potential (MEP) were used to evaluate the upper limb movement function and daily life activity. Results: There were no significant differences between experiment and control group in the indexes, including FMA, WMFT, and MBI scores, before the intervention. However, after 8 weeks treatments, these indexes were improved significantly. MEP latency and center-motion conduction time (CMCT) decreased from 23.82 ± 2.16 and 11.15 ± 1.68 to 22.69 ± 2.11 and 10.12 ± 1.46 ms. MEP amplitude increased from 0.61 ± 0.22 to 1.25 ± 0.38 mV. A remarkable relationship between the evaluations indexes of MEP and FMA was found. Conclusions: Combination of motion observation and traditional upper limb rehabilitation treatment technology can significantly elevate the movement function of cerebral infarction patients in subacute seizure phase with upper limb dysfunction, which expanded the application range of motion observation therapy and provided an effective therapy strategy for upper extremities hemiplegia in stroke patients.
Referred phantom sensations are frequently reported following a peripheral injury. However, very few cases describe such sensations of the ear, and it remains unclear how the aural nerve territory can be remapped to one specific peripheral nerve region. We report on a patient with brachial plexus avulsion who underwent sensory testing and was asked to report the location of the stimulated site and any other sensations experienced. The patient spontaneously described the sensation of his arm being separate from his body. Despite visual input, he felt that his fist was closed, with his thumb pointing inward. Importantly, he felt clear and reproducible sensations from the affected arm when the ipsilateral ear was touched. These referred sensations were noted just 15 days after sustaining the injury. The arm nerve territory was systematically remapped to a specific aural nerve territory by applying both manual and electrical stimulation. Stimulation of the external ear, which is innervated by the vagus nerve, showed high spatial specificity for the dorsal and volar skin surfaces of the limb, and clearly delineated digits. Somatosensory-evoked potentials indicated that cortical adaptation in the somatosensory stream transferred a spatially organized map of the limb to the skin of the outer ear. This referral of sensations to the ear, as distinct from the face, provides evidence of highly specific topographical reorganization of the central nervous system following peripheral injury. Rapid map changes in the phantom sensation to the ear as a function of stimulation of vagus nerve suggest that the reorganization process can occur in cortex rather than in the brainstem.
Introduction Occupational therapists have been using various preparatory methods as part of the treatment sessions to prepare clients for occupational performance and participation in occupation. Studies have shown sensory stimulation both activates brain areas inducing cortical reorganization and modulates motor cortical excitability for the stimulated afferents, hence re-establishing the disrupted sensorimotor loop due to stroke. This pilot investigates the potential effects of using multisensory stimulation as a preparatory method prior to conventional training (CT) on upper-extremity motor recovery and self-care function in stroke patients. Method This was a quasi-randomized controlled pilot. Twelve participants (age in years = 67.17 + /−11.29) with upper extremity motor deficits were randomly allocated to multisensory therapy (n = 6) or conventional (n = 6) groups for 12-week training. Assessments were conducted at baseline and post-intervention using Fugl-Meyer Assessment of Motor Recovery after Stroke (FMA), Manual Muscle Testing (MMT), Functional Test for the Hemiplegic Upper Extremity (Hong Kong version FTHUE-HK) and Modified Barthel Index (MBI). Results Significant between-group differences were shown in FMA ( p = 0.003), FTHUE-HK ( p = 0.028) and MMT ( p = 0.034). Conclusion Multisensory stimulation could be used as a preparatory method prior to CT in improving upper extremity motor recovery in stroke rehabilitation. Further well-designed larger scale studies are needed to validate the potential benefits of this application.
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.
Gestural apraxia was first described in 1905 by Hugo Karl Liepmann. While his description is still used, the actual terms are often confusing. The cognitive approach using models proposes thinking of the condition in terms of production and conceptual knowledge. The underlying cognitive processes are still being debated, as are also the optimal ways to assess them. Several neuroimaging studies have revealed the involvement of a left-lateralized frontoparietal network, with preferential activation of the superior parietal lobe, intraparietal sulcus and inferior parietal cortex. The presence of apraxia after a stroke is prevalent, and the incidence is sufficient to propose rehabilitation.