Available via license: CC BY
Content may be subject to copyright.
PERSPECTIVE
published: 03 April 2019
doi: 10.3389/fneur.2019.00309
Frontiers in Neurology | www.frontiersin.org 1April 2019 | Volume 10 | Article 309
Edited by:
Giorgio Sandrini,
University of Pavia, Italy
Reviewed by:
Marianna Capecci,
Polytechnical University of Marche,
Italy
Marialuisa Gandolfi,
University of Verona, Italy
*Correspondence:
Mariella Pazzaglia
mariella.pazzaglia@uniroma1.it
Specialty section:
This article was submitted to
Neurorehabilitation,
a section of the journal
Frontiers in Neurology
Received: 30 August 2018
Accepted: 11 March 2019
Published: 03 April 2019
Citation:
Pazzaglia M and Galli G (2019) Action
Observation for Neurorehabilitation in
Apraxia. Front. Neurol. 10:309.
doi: 10.3389/fneur.2019.00309
Action Observation for
Neurorehabilitation in Apraxia
Mariella Pazzaglia 1,2
*and Giulia Galli 2
1Department of Psychology, University of Rome “La Sapienza,” Rome, Italy, 2IRCCS Fondazione Santa Lucia, Rome, Italy
Neurorehabilitation and brain stimulation studies of post-stroke patients suggest that
action-observation effects can lead to rapid improvements in the recovery of motor
functions and long-term motor cortical reorganization. Apraxia is a clinically important
disorder characterized by marked impairment in representing and performing skillful
movements [gestures], which limits many daily activities and impedes independent
functioning. Recent clinical research has revealed errors of visuo-motor integration in
patients with apraxia. This paper presents a rehabilitative perspective focusing on the
possibility of action observation as a therapeutic treatment for patients with apraxia. This
perspective also outlines impacts on neurorehabilitation and brain repair following the
reinforcement of the perceptual-motor coupling. To date, interventions based primarily
on action observation in apraxia have not been undertaken.
Keywords: apraxia, action recognition, action execution, mirror activity, neurorehabilitation
INTRODUCTION
Apraxia encompasses a broad spectrum of higher-order purposeful movement disorders (1) and
is most often associated with neurological damage to left-hemisphere (2). The accepted definition
of apraxia includes deficits in performing, imitating, and recognizing skilled actions involved in
the intentional movements, colloquially referred to as gestures (3). Pathological conditions such as
apraxia result from an inability to evince the concept of specific actions (4) or to execute related
motor programs (5). Classically, apraxia is diagnosed when a patient presents with an inability
to execute gestures in response to verbal commands or imitate with different effectors (mouth,
hand, or foot) (4), including movements involving the non-paretic limb ipsilateral to the lesion[s].
Although apraxia primarily affects motor activities, studies report that higher impairment levels
may be related to visuo-motor integration (6). Recent evidence supports the notion that apraxia
influences skilled acts in the environment, interferes with independent functioning, impedes daily
activities, and affects the performance of routine self-care (7,8); that is, persons may have difficulty
brushing their teeth (9), eating (7), preparing food (10), and getting dressed (11). As a consequence,
patients with apraxia can develop severe anxiety and reductions in the spontaneous use of social
gestures (12), leading to isolation and depression (13) and consequent delays in returning to
work (14).
Almost 50% of patients with left-hemispheric stroke (15) and ∼35% of patients with Alzheimer’s
disease and corticobasal degeneration (16–18) develop apraxia that persists after illness onset
and affects functional abilities. Research to aid in the development and optimization of apraxia
neurorehabilitation is crucial. Several approaches for the treatment of apraxia deficits are currently
in practice [for a review see (19,20)], including verbal (21) or pictorial (22) facilitation and the
use of physical cues based on repetitive behavioral-training programs with gesture-production
exercises. The errorless completion method represents another recent approach (23). Autonomy in
Pazzaglia and Galli Neurorehabilitation and Apraxia
activities of daily living tends to be underestimated (24),
and rehabilitation studies remain limited due to the nature
of disturbances to automatic/voluntary dissociations (i.e., an
ability to execute actions only in natural settings). To date,
no rehabilitation treatment or therapeutic possibilities based
primary on action observation has been studied in apraxia.
THE VALUE OF ACTION OBSERVATION IN
TREATING APRAXIA
Language disorders among patients with apraxia who suffer from
concomitant aphasia suggest that defects in gesture imitation,
rather than gestures in response to verbal commands, are more
sensitive indicators of apraxia (25). Goldenberg has proposed
that imitation apraxia could be primarily considered a deficit of
perceptual analysis (26). Evidence from several studies indicates
that perceptual and motor codes are closely associated (27,
28) and that patients with apraxia may be defective both in
performing motor acts and in the perceptual code necessary to
represent the appropriate gesture. Sunderland and Sluman have
shown, for example, that problems orienting a spoon in a bean-
spooning task suggest an inability to remember the correct action
and to judge the correctness of the perceived action (29).
Although apraxia is commonly considered a motor
impairment, deficits in intact gestural perception are not
uncommon, occurring in 33% of one sample (30). Such
patients, who exhibit deficits in the execution of actions,
also commit errors when judging between correctly and
incorrectly performed acts (30–32), understanding the meaning
of pantomimes (33,34), discriminating among action-related
sounds (35,36), matching photographs of gestures (26), engaging
visuo-motor temporal integration (6), and predicting incoming
observed movements (37,38).
Movement-execution effects in apraxia thus are not purely
motor processes and visual representations of given actions may
influence the actions’ execution by visuo-motor transfer (39). The
integrity of gesture representations has important implications
for rehabilitation strategies (40). The spatial and temporal use
of a body part for the planning of a tool-related action and
the imitation of others’ actions involve an inherent perceptual
component, which can be disturbed following apraxia onset. As
a result, modern assessments of apraxia include evaluations of
gesture understanding (32,41).
VISUAL-MOTOR STRATEGIES IN THE
REHABILITATION OF PATIENTS WITH
LIMB APRAXIA
The notion of common representations for both executed and
observed actions is of considerable interest in the applied field
of stroke neurorehabilitation (42,43). Despite the use of state-
of-the-art apraxia-evaluation batteries (44) to explore perceptual
deficits in the understanding of actions in patients with apraxia,
few studies have proposed new rehabilitation programs that
include elements of both observation and execution of actions.
Smania et al.’s (45) clinical examinations of 43 left brain-
damaged patients with apraxia revealed defective performances
in gesture execution and imitation, as well as in the recognition
and identification of transitive and intransitive gestures. For their
study, approximately half of the patients received training in
ecological action production and comprehension; the other half
underwent conventional language rehabilitation for the same
number of treatment hours. The training, which combined the
observation and execution of observed actions, consisted of three
progressive phases, each characterized by increasing degrees of
difficulty, obtained by phased reductions of facilitation cues as
performance improved. After ∼30 sessions, therapists recorded
significant improvements: approximately 50% improvement in
the ADL scale and an average of 40% in the praxis test (22). When
only considering apraxia patients with cortical lesions primarily
in the fronto-parietal network, the improvement was even greater
(45). No significant performance changes were observed in the
outcome measures of control patients who did not undergo
specific programs of gesture production/observation exercises.
Interestingly, authors reported a significant improvement in
gesture recognition performance after the apraxia treatment,
and a correlation was found between gesture comprehension
tests and the ADL questionnaire (ADL-gesture comprehension:
R=0.37, p=0.034) (22). These results suggest that the positive
effects of this rehabilitative approach in apraxia require parity
in the treatment of both the motor and the perceptual aspects
of action processing (45). Of note, beneficial effects persisted
for at least 2 months and extended to the daily living activities
even of untreated actions, helping patients attain functional
independence from their caregivers (22).
Goldenberg and Hagmann (9) developed a particularly
successful restorative method in which training comprised two
different methods. The first aimed at helping patients to learn and
correctly execute complete activities, with therapists providing
different support at all clinical steps (e.g., by demonstrating
gesture execution and asking patients to imitate them), and
reducing the support only when patients were able to perform
these steps on their own. The second aimed at directing patients’
attention to the functional meaning of objects’ individual features
and details, critical for various actions. This two-step procedure
ensured a double reinforcement of the action’s perceptual-
motor code: the first online within the simultaneity of the
demonstration and the second off-line as a delayed imitation.
The combination of these two methods led to significant
improvements in trained ADL, but virtually no generalization of
training effects was observed between trained and non-trained
activities. The therapy’s success was preserved among those
patients who performed the activities at home but not among
those who did not. In a subsequent study (46), the authors
developed a slightly different variant to previous approaches
in which patients carried out entire activities with a minimum
of errors. In this approach, the functional commonalities
between different objects were emphasized by providing verbal
instructions and visual and gestural support. Effects of these
treatments lasted up to 3 months after the treatment ended.
Compensatory treatment indicate that the patients showed
large improvements in ADL functioning after rehabilitative
Frontiers in Neurology | www.frontiersin.org 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 (47–50).
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
(64–86), patients with Parkinson’s disease (87–92), children
with cerebral palsy (93–97) and elderly individuals with reduced
cognitive abilities (98). Electrophysiological studies have also
reported positive effects of action observation on the recovery
of motor functions after acute and chronic stroke (71,99).
This non-invasive, inexpensive, user-friendly approach works
more quickly on biological effectors (mouth, limbs, and trunk),
promoting better and faster recovery.
A NEURAL SUBSTRATE FOR ACTION
OBSERVATION AND EXECUTION IN
APRAXIA REHABILITATION
The inextricable link between action perception and execution
was first posited in the ideomotor theory, which has been
validated through delineation of the brain network, known as
the mirror neuron system (MNS). Inspired by single-cell (“mirror
neuron”) recordings in monkeys (100,101), many neuroimaging
and neurophysiological studies have suggested that the adult
human brain is equipped with neural systems and mechanisms
that represent both the visual perception and execution of actions
in a common format (102). Action deficits among the patients
with apraxia may be described at multiple levels. While these
levels partially overlap, four levels of hierarchical modeling at
which an MNS mechanism can support an observed action
(42,103) are as follows:
(i) kinematic: Patients with apraxia frequently present with
abnormalities in kinematic movements in the form of motor
patterns that are slower, shorter, and less vertical than those
of individuals without apraxia (104);
(ii) motor: Limb apraxia interferes with the selection and
control of the hand-muscle activity (105). Moreover,
it interferes with the formation of appropriate hand
configurations for using objects (106);
(iii) goal: Understanding the immediate purpose of an action is
impeded; for example, patients with apraxia are impaired
access to mental representation of tool use (33);
(iv) intention: Patients present with an altered ability to monitor
the early planning phases of their own actions (107).
The cortical areas have been shown to contain mirror neurons
that are often described as a part of an integrated sensorimotor
information system underpinned by neural activity in the frontal
(103), parietal (108), and superior temporal sulcus areas. This
system is called the action observation network (AON) (109).
In humans, these cortical regions mediate the observation of
actions that form a part of the observer’s motor repertoire (41).
They also contribute to the imitation (110) and comprehension
(111) of these movements, and are involved in skill acquisition
(112). Lesion symptom mapping studies have reported gestural
deficits in patients with apraxia, which are most frequently
apparent following lesions in the inferior frontal lobe (30,113–
116), and in supramarginal and angular gyrus (37,113,115,
117) of the left hemisphere. However, apraxia has also been
observed in patients with damage in posterior middle temporal
lobe, anterior temporal lobe (37,113,115,117), occipital, and
subcortical regions (6,118,119). Despite the damaged neural
substrate was not constant across all the studies, it includes the
areas that are considered crucial for the AON. Undoubtedly, the
mirror neurons just provide a part of the complex information
for achieving action comprehension while action recognition
and production occur simultaneously by accessing the same
neural representations. However, as posited by the influential
cognitive neuropsychological models of apraxia (120,121) and
demonstrated by various clinical studies (121–124), 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 | www.frontiersin.org 3April 2019 | Volume 10 | Article 309
Pazzaglia and Galli Neurorehabilitation and Apraxia
TABLE 1 | Apraxia intervention studies.
References Number of participants Treatment
duration
Type of
action
Control Intervention Perceptual aspects
of training
Improvements in
experimental group
No effect
Experimental
group
Control
group
van Heugten
et al. (47)
33 30 min for 12
weeks
Everyday
activities
Strategy training Observation of picture
sequences Imagination
ADL Barthel Index
Apraxia Test Motor
functioning
Goldenberg and
Hagmann (9)
15 5 weeks Three
activities from
the domains
eating,
dressing, and
grooming
Direct training of
the activity:
errorless
completion of the
activity
The patients perform
action immediately after
observing the
therapist’s
demonstration
10 patients improved
on all three trained
activities
6 months later,
improvement is
not maintained
without practice
Smania et al. (45) 6 7 35 sessions,
three per
week
Transitive
action
Intransitive
action
Imitation
Aphasia
therapy
Gesture
recognition
Gesture execution
Observation of picture
(context, object)
Gesture recognition
Imitation
Apraxia Test Gesture
recognition
Verbal
comprehension
Oral apraxia
Donkervoort et al.
(48)
42 48 8 weeks Everyday
activities
Occupational
therapy
Strategy training Observation of picture
sequences Imagination
ADL Barthel Index Apraxia Test ADL
untrained
Goldenberg et al.
(46)
6 4 weeks Four everyday
activities
Explorative training
vs. Direct training
of the activity
The patients perform
action immediately after
observing the
therapist’s
demonstration
Direct training of activity
reduced errors and
amount of assistance
Exploration
training had no
effect on
performance
Smania et al. (22) 18 15 30 sessions,
three per
week
Transitive
action
Intransitive
action
Imitation
Aphasia
therapy
Gesture
recognition
Gesture execution
Observation of picture
(context, object)
Gesture recognition
Imitation
Apraxia Test Gesture
recognition ADL
Verbal
comprehension
Oral apraxia
Geusgens et al.
(50)
56 57 25 sessions,
8 weeks
Action of daily
living
Occupational
therapy
Strategy training Observation of picture
sequences
ADL untrained
Geusgens et al.
(49)
29 25 sessions,
8 weeks
Action of daily
living
Strategy training Observation of picture
sequences
Apraxia Test ADL
trained ADL untrained
Barthel Index
Functional Motor
Test
Bolognini et al.
(51)
6 6 3 sessions,
10 min
Limb gesture
imitation
Sham
stimulation
Anodal tDCS on
the left parietal
cortex
Imitation (observation
+execution)
Imitation execution tDCS on the motor
cortex
Frontiers in Neurology | www.frontiersin.org 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.
NEUROREHABILITATION AND BRAIN
REPAIR AFTER APRAXIA
The behavioral success of rehabilitation methods based on the
principle of action observation should promote reorganization
by adaptive plasticity at the neural level (128,129). Functional
reorganization clearly depends on the residual neural integrity
of efferent (motor) and afferent (sensory) information, which
leads to improved treatment outcomes among some apraxia
patients but not for others. In this perspective, we considered
three possible sources of informational content for how
neurorehabilitation and brain repair after apraxia works: injury
site, elapsed time after apraxia onset, and lesion size.
The first factor to consider is the location of the infarct,
which can ultimately determine the outcome of rehabilitation
treatment. Whereas, lesions of the frontal and parietal cortices
in the left hemisphere have been shown to primarily disrupt
gesture production in patients with apraxia (2), no clear
correlation has been found between lesion location and
impairment in visual gesture representation. Apraxic patients
with cortical lesions—but not those with subcortical lesions—
cannot comprehend the meaning of gestures (130). In rare
cases, a lesion in the left occipito-temporal cortex may also
critically hamper the ability to recognize gestures in patients
with apraxia (120,131). Patients with parietal lesions have also
been reported to exhibit significant impairments in executing
gestures but only slight impairments in understanding those
performed by others (132). The neural specificity of this
disturbed typology may explain why certain patients with
apraxia are able to comprehend the meaning of gestures
despite being unable to perform them themselves. Accordingly,
single-case and group studies report dissociations between
action execution and representation and the underpinning
damaged neural substrate (121–124). 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 | www.frontiersin.org 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.
CONCLUSION
While research on the relationship between observed and
executed actions in apraxia neurorehabilitation has a short
history, it has already provided insights about the positive effect
of a visual-motor training. The observation of actions through
a process of visual retrieval may help in the selection of the
most probable action, providing a powerful tool for overcoming
intentional motor-gestural difficulties (55). Moreover, tailored
interventions based on individual’s ability to acquire new (or
relearn old) motor-memory traces through multisensory [i.e.,
auditory (35,147), olfactory (148,149), and tactile (150–
155)] feedback may be the most promising approach for a
normal temporal integration action (156,157). Multisensory
stimulation can activate multiple cortical brain structures,
inducing cortical reorganization and modulating motor cortical
excitability for the stimulated afferents (158,159). Results
are encouraging, but it is important to emphasize that this
hypothesis does not imply that all deficits in apraxia can
be treated by action observation therapy. Rather, we believe
that action observation might be a therapeutic option for
improving praxis function among certain specific typologies
of patients.
AUTHOR CONTRIBUTIONS
MP: study concept and design, manuscript development, and
writing. GG: contributed to the writing of the manuscript.
FUNDING
This work was supported by the Italian Ministry of Health
(RF-2018-12365682 to MP).
Frontiers in Neurology | www.frontiersin.org 6April 2019 | Volume 10 | Article 309
Pazzaglia and Galli Neurorehabilitation and Apraxia
REFERENCES
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 | www.frontiersin.org 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 | www.frontiersin.org 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.
5281.1564
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 | www.frontiersin.org 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/
4843985
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 | www.frontiersin.org 10 April 2019 | Volume 10 | Article 309