Limb Apraxias and Related Disorders

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Chapter 10 Limb Apraxias and Related Disorders

Apraxia is an inability to correctly perform learned skilled movements. In the limb apraxias, there is an inability to correctly execute these movements in an arm or hand owing to neurological dysfunction. Apraxia is a cognitive deficit in motor programming and results in errors of either the spatiotemporal processing of the movements or in the content of the actions. In the context of an apraxia examination, these errors can help distinguish the major types of limb apraxias.

A first step in recognizing the limb apraxias is distinguishing them from other causes of impaired movement. First of all, it is not apraxia if the impaired movements result from elementary motor deficits such as weakness, hemipareses, spasticity, ataxia, or extrapyramidal disturbances. Second, apraxia is distinguishable from impaired movements due to primary sensory deficits, hemispatial neglect, spatial or object agnosia, or other complex visual disorder. Third, apraxia is distinct from abnormal movements or postures such as tremor, myoclonus, choreoathetosis, or dystonic posturing. Finally, it is not apraxia if the impaired movements result from other cognitive disorders involving attention, memory, language comprehension, or executive functions (Leiguarda and Marsden, 2000). Although these sensorimotor and cognitive disorders may coexist with limb apraxia, the clinician must first ascertain whether they account for the patient’s inability to perform learned skilled movements.

Limb apraxia is not rare or insignificant. Apraxia occurs in about 50% to 80% of patients with left hemisphere lesions and can persist as a chronic deficit in 40% to 50% of these. Limb apraxia often results in major functional impairment, even when subtle, as it affects critical movements of the arms, hands, and fingers. Limb apraxia correlates with the level of caregiver dependence and greater need for help with activities of daily living (ADLs). It can also interfere with rehabilitation and therapy, including occupational therapy, physical therapy, and the use of gestural communication in aphasia rehabilitation.

Despite its importance, clinicians often fail to recognize limb apraxia. In many left hemisphere strokes, right hemiparesis masks the presence of right limb apraxia, and the assumption of normal non-dominant hand clumsiness masks the presence of left limb apraxia. Even when there are no masking factors, the presence of limb apraxia may still go undetected. Many examiners do not evaluate patients for limb apraxia, do not know how to test for apraxia, or cannot recognize the spatiotemporal or content errors produced by this condition. Yet apraxia is part of the diagnostic criteria of Alzheimer disease and corticobasal syndrome, as well as a manifestation of many other disorders.

This chapter is about the limb apraxias. The term apraxia occurs broadly in neurology and is usually interchangeable with dyspraxia. Apraxia describes non-learned motor dysfunctions including oculomotor movements, gait initiation (magnetic apraxia), and eyelid opening. It also describes skilled motor tasks that are dependent on visuospatial processing, including optic, constructional, and dressing apraxia. Apraxia is used as well for conditions that are more clearly consistent with the definition of disturbances in learned skilled movements but involve body parts other than the limbs, including orobucchal-facial and speech apraxias. These clinical entities are not included in this chapter, because they are either not limb apraxias or not disorders of “praxis” in the sense of disturbances in learned skilled movements (Zadikoff and Lang, 2005). This chapter focuses on the seven major limb apraxias of the upper extremities, where apraxia is most evident. They include ideomotor apraxia, parietal variant; ideomotor apraxia, disconnection variant; dissociation apraxia; ideational apraxia; and conceptual apraxia. Also included is limb-kinetic apraxia, a disorder that some argue is not a true apraxia, but instead a more basic disturbance in fine motor movements. Callosal apraxias comprise a separate category because of their unique unilateral and varied manifestations.

Historical Perspective

Many clinicians and investigators helped develop the current concept of limb apraxia. In 1866, John Hughlings Jackson probably recognized the clinical phenomenon of apraxia in a patient (Pearce, 2009). Jackson observed that the patient had “power in his muscles and in the centres for coordination of muscular groups, but he – the whole man, or the ‘will’ – cannot set them agoing.” In 1870, Carl Maria Finkelnburg used “asymbolia” to describe the clumsy and incomprehensible communicative gestures in aphasics, and in 1890, Meynert distinguished motor asymbolia from decreased motor “images” for movement. In 1899, D. De Buck used “parakinesia” to describe a patient who “though retaining the concepts for her actions, did not succeed in awakening the corresponding kinetic image.” By this time, the stage was set for Hugo Karl Liepmann’s seminal model of the limb apraxias.

In the early 1900s, Liepmann published a series of papers that led to the contemporary concept of limb apraxias. He proposed that the execution of purposeful movements could be divided into three steps (Goldenberg, 2003). First is the retrieval of the spatial and temporal representation or “movement formulas” of the intended action from the left hemisphere. Second is the transfer and association of these movement formulas via cortical connections with the “innervatory patterns” or motor programs located in the left “sensomotorium” (which includes premotor and supplementary motor areas). Third is the transmission of the information to the left primary motor cortex for performance of the intended actions in the right limb. Finally, in order for the left limb to perform the movements, the information traverses the corpus callosum to the right sensomotorium to activate the right primary motor cortex. Using Heymann Steinthal’s term of “apraxia,” Liepmann classified disturbances in these connections as “ideational, ideo-kinetic (melokinetic), and limb-kinetic apraxia.” Over the years, this classification nomenclature has evolved and the application of these terms has shifted, but Liepmann’s basic formulation of apraxia has persisted to the present day.

A Model for Praxis

The left parietal region retains its central role of converting mental images of intended action into motor execution (Heilman and Rothi, 2003) (Fig. 10.1). The inferior parietal lobule contains the spatial and temporal movement programs (praxicons, visuokinesthetic motor engrams, or movement formulas) needed to carry out learned skilled movements. Multiple input modalities including visual, verbal-auditory, and tactile can activate these movement formulas. Cells in the inferior parietal lobule fire selectively in response to hand movements, visually presented information about object size and shape, or the actual manipulation of objects (Rizzolatti et al., 1998), and functional neuroimaging studies show activity of this region in response to recognition of actions associated with object or tool use (transitive actions) (Damasio et al., 2001). The right parietal lobe participates in the integration of visual information and upper-extremity movement. In addition to movement formulas, the left parietal region appears to contain action semantics and conceptual systems such as tool action, tool-object association information, and general principles of tool use (Goldenberg and Spatt, 2009; Ochipa et al., 1992). If a movement involves the use of a tool or object, action semantics specify knowledge of tool action (turning, pounding, etc.) and the knowledge of which tool or object to use to choose for a task (Leiguarda and Marsden, 2000).

In the premotor region, the supplementary motor area (SMA) translates the movement formulas into motor programs before sending them on to primary motor cortex (Roy and Square, 1985). The SMA, which is involved in complex movements of the upper extremities, receives projections from parietal neurons and in turn projects axons to motor neurons in the primary motor cortex. The SMA programs a specific order of movements and is involved in bimanual coordination. It translates these time-space movement formulas to specific motor programs that activate the motor neurons such that the contralateral extremity moves in the proscribed spatial trajectory and timing. For movements in the opposite extremity, the brain further conveys these programs across the corpus callosum to the opposite premotor cortex and activates the motor neurons for the desired contralateral extremity movements.

Beyond this traditional model for praxis, apraxia may result from damage in other regions including the prefrontal cortex, right hemisphere, basal ganglia (putamen and globus pallidus), thalamus, and their white-matter connections. The prefrontal region participates in sequencing multiple arm, hand, and finger movements. The right parietal region participates in performing nonpurposeful movements. Although the left inferior parietal lobule is more active than the right during action imagery and actual discrimination of nonpurposeful gestures, the right parietal region is more active during imitation and when these gestures consist of finger postures (Buccino et al., 2001; Hermsdorfer et al., 2001). The role of basal ganglia and thalamus is less clear, but they function as part of cortical-subcortical motor loops. Apraxia could, theoretically, result from damage to any of these areas outside the traditional model of praxis.

Classification of Limb Apraxias

Beginning with Liepmann, there have been multiple attempts to classify and define the limb apraxias (Hanna-Pladdy and Rothi, 2001). The classification presented here is based on the seminal work of Heilman and associates, who have significantly contributed to the understanding of the limb apraxias (Heilman and Rothi, 2003). Depending on the location of the lesion, the patient has different patterns of ability to imitate and recognize gestures, perform sequential movements, and do fine motor activities (Fig. 10.2). The presence of production and content errors further characterize the subtypes of limb apraxia.

Ideomotor Apraxia, Parietal Variant

The parietal variant of ideomotor apraxia may be the most common and prototypical limb apraxia. Disruption of the movement formulas in the inferior parietal lobule impairs skilled movements on command and to imitation, as well as the recognition of gestures (see Fig. 10.2, A). Patients make spatial and temporal errors while producing movements. There is a failure to adopt the correct posture or orientation of the arm and hand or to move the limb correctly in space and at the correct speeds. Spatial errors involve the configuration of the hand and fingers, the proper orientation of the limb to the tool or object, and the spatial trajectory of the motion. A major distinguishing feature of the parietal variant of ideomotor apraxia is difficulty recognizing or identifying gestures, implicating damage to the praxicons, visuokinesthetic motor engrams, or movement formulas themselves.

Ideomotor Apraxia, Disconnection Variant

The disconnection variant of ideomotor apraxia results from disruptions of motor programs in the SMA or in their intra- and interhemispheric connections (Heilman and Watson, 2008). This form of ideomotor apraxia is a disconnection of an intact parietal region from the pathways to primary motor cortices. These lesions result in impaired pantomime to verbal commands, impaired imitation of gestures, and the presence of spatiotemporal production errors. The movement formulas themselves are preserved, but in contrast to the parietal variant of ideomotor apraxia, these patients can recognize and identify gestures. The lesions lie along the route from the left inferior parietal cortex to primary motor cortices (see Fig. 10.2, B). Although SMA lesions tend to affect both upper extremities, if the SMA lesion is limited to the right, apraxia may be limited to the left upper extremity.

Callosal Apraxia

Several limb apraxia syndromes can result from callosal lesions (see Fig. 10.2, G). What distinguishes these patients is that their apraxia is confined to the non-dominant limb, usually the left arm or hand in right-handed individuals. The right limb may be affected in left-handed individuals, or they may have a similar lateralization as right-handers. Liepmann and others described left-sided disconnection-variant ideomotor apraxia due to callosal lesions and strokes (Heilman and Watson, 2008). These patients cannot pantomime with their left hand to verbal command or imitate but can recognize and identify gestures. Others described left-sided dissociative apraxia due to callosal lesions (Gazzaniga et al., 1967; Geschwind and Kaplan, 1962). Patients who have had surgical disconnection of the corpus callosum could not gesture normally to command with their left arm and hand but performed well with imitation and actual tools. Some patients have had a combination of both ideomotor and dissociative apraxia of their left arm and hand manifested by unrecognizable movements on verbal command and spatiotemporal errors on imitation. Other patients have a callosal “alien limb” with independent movements of the non-dominant limb, sometimes with “diagonistic apraxia” or the intermanual conflict of the hands acting in opposition to each other. The classic example of this is the split-brain patient who has undergone a corpus callosotomy who finds that his or her left hand is unbuttoning his shirt or blouse while the right one is trying to button it. Finally, there is a rare description of callosal lesions resulting in conceptual apraxia, indicating that conceptual knowledge as well as movement formulas have lateralized representations, and that such representations are contralateral to the preferred hand (Heilman et al., 1997).

Testing for Limb Apraxias

Apraxia testing involves a systematic approach (Box 10.1). Prior to testing of praxis, a neurological examination excludes the presence of significant motor, sensory, or cognitive disorders that could explain the inability to perform learned skilled movements. First, the testing of praxis itself begins with asking the patient to pantomime to command. The movements are transitive (associated with tool or instrument use) and intransitive (associated with communicative gestures such as waving goodbye). For transitive movements, the examiner asks the patient to demonstrate how to comb their hair, brush their teeth, or use a pair of scissors. For intransitive movements, the examiner asks the patient to demonstrate how to wave goodbye, beckon somebody to come, or hitchhike. The testing involves the right and left limb independently. The examiner observes the patient for the presence of temporal-spatial or content errors. Second, if the patient has difficulty pantomiming movements, the examiner tests their ability to imitate gestures. For gesture imitation, the examiner performs both transitive and intransitive movements and asks the patient to copy the movements. Third, for gesture knowledge, the examiner performs the same transitive and intransitive gestures and asks the patient to identify the gesture. The patient must identify the gesture and discriminate between those that are well and poorly performed. Fourth, the patient must perform tasks that require several motor acts in sequence, such as making a sandwich or preparing a letter for mailing. Fifth, the examiner shows the patient pictures of tools or objects or the actual tools or objects themselves. The examiner then requests that the patient pantomime the action associated with the tool or object. Finally, the examiner checks for fine finger movements by asking the patient to do repetitive tapping, picking up a coin with a pincer grasp, and twirling the coin. Additional impairment in the patient’s ability to use real objects indicates marked severity of the limb apraxia. The pattern of deficits will determine the types of apraxia (Table 10.1). Specialists in occupational therapy, physical therapy, speech pathology, and neuropsychology can further assess and quantify the deficits in limb apraxia using instruments like the Apraxia Battery for Adults-2 and the Florida Apraxia Battery (Power et al., 2010).

Box 10.1 The Examination for Limb Apraxias

I. DOMINANT UPPER EXTREMITY

a. Transitive actions:

II. NON-DOMINANT UPPER EXTREMITY

The examiner repeats the same procedures as for the dominant upper extremity.

Testing for Ideomotor Apraxia, Parietal and Disconnection Variants

Patients with the ideomotor apraxias cannot pantomime to command or imitate the examiner’s gestures. These patients improve only partially with intransitive acts, imitation, and real object use. Ideomotor apraxia results in spatiotemporal errors in the positioning and orientation of the arm, hand, and fingers to the target and in the timing of the movements, but the goal of the action is still recognizable. In addition to poor positioning of the limb in relation to an imagined object, patients with ideomotor apraxia have an incorrect trajectory of their limb through space owing to poor coordination of multiple joint movements. Patients with ideomotor apraxia also have hesitant, stuttered movements rather than smooth, effortless ones. Unlike patients with the parietal variant of ideomotor apraxia, patients with the disconnection variant can both comprehend gestures and pantomimes and discriminate between correctly and incorrectly performed pantomimes.

On attempting to pantomime, patients with ideomotor apraxia may substitute a body part for the tool or object (Raymer et al., 1997). For example, when attempting to pantomime combing their hair or brushing their teeth, they substitute their fingers for the comb or toothbrush. Normal subjects may make the same errors, so the examiner should ask patients not to substitute their fingers or other body parts but to pantomime using a “pretend tool.” Patients with ideomotor apraxia may not improve with these instructions and continue to make body-part substitution errors. The substitution of a body part for a tool or object activates the right inferior parietal lobe, hence patients with ideomotor apraxia with left parietal injury appear to be using their normal right parietal lobe in order to pantomime gestures (Ohgami et al., 2004).

Pathophysiology of Limb Apraxias

Ideomotor apraxia is associated with lesions in a variety of structures including the inferior parietal lobe, the frontal lobe, and the premotor areas, particularly the SMA. There are reports of ideomotor apraxia due to subcortical lesions in the basal ganglia (caudate-putamen), thalamus (pulvinar), and associated white-matter tracts including the corpus callosum. Limb apraxias can be caused by a variety of central nervous system disorders that affect these regions. The different forms of limb apraxia result from cerebrovascular lesions, especially right middle cerebral artery strokes with right hemiparesis. There may be left-sided limb apraxia in these patients. Right anterior cerebral artery strokes and paramedian lesions could produce ideomotor apraxia, disconnection variant. Ideomotor apraxia and limb-kinetic apraxia can be the initial or presenting manifestation of disorders such as corticobasal syndrome, primary progressive aphasia, or parietal-variant Alzheimer disease (Rohrer et al., 2010). Tumors, traumatic brain injury, infections, and other pathologies can also lead to limb apraxias.

There are effects of hemispheric specialization and handedness on praxis. Early investigators proposed that handedness was related to the hemispheric laterality of the movement formulas. The greatest evidence is for the left hemisphere localization of the movement formulas. Studies using functional imaging have provided converging evidence that in people who are right-handed, it is the left inferior parietallobe that appears to store the movement representation needed for learned skilled movements (Muhlau et al., 2005). Left-handed people, however, may demonstrate an ideomotor apraxia from a right hemisphere lesion, because their movement formulas are stored in their right hemisphere. It is not unusual to see right-handed patients with large left hemisphere lesions who are not apraxic, and there are rare reports of right-handed patients with right hemisphere lesions and limb apraxia. These findings suggest that hand preference is not entirely determined by the laterality of the movement formulas, and praxis and handedness can be dissociated.

Rehabilitation for Limb Apraxias

Because many instrumental and routine ADLs depend on learned skilled movements, patients with limb apraxia usually have impaired functional abilities. The presence of limb apraxia, more than any other neuropsychological disorder, correlates with the level of caregiver assistance required 6 months after a stroke, whereas the absence of apraxia is a significant predictor of return to work after a stroke (Saeki et al., 1995). The treatment of limb apraxia is therefore important for improving the quality of life of the patient.

Even though many treatments have been studied, none has emerged as the standard. There are no effective pharmacotherapies for limb apraxia, and treatments primarily involve rehabilitation strategies. Buxbaum and associates (2008) surveyed the literature on the rehabilitation of limb apraxia and identified 10 studies with 10 treatment strategies: multiple cues, error type reduction, 6-stage task hierarchy, conductive education, strategy training, transitive/intransitive gesture training, rehabilitative treatment, error completion, exploration training, and combined error completion and exploration training. Most of these approaches emphasize cueing with multiple modalities, with verbal, visual, and tactile inputs, repetitive learning, and feedback and correction of errors. Patients with post-stroke apraxia have had generalization of cognitive strategy training to other activities of daily living (Geusgens et al., 2006), but others have not (Bickerton et al., 2006). Although most studies have shown positive treatment effects, fewer studies have demonstrated the effects to be generalizable compared to those that have not. It is also unclear whether the benefits can be sustained long term. In sum, patients can learn and produce new gestures, but the newly learned gestures may not generalize well to contexts outside the rehabilitation setting. Nevertheless, some patients with ideomotor apraxia have improved with gesture-production exercises (Smania et al., 2000), and patients with apraxia would benefit from referral to a rehabilitation specialist with experience in treating apraxias.

Additional important interventions for the management of limb apraxias involve making environmental changes. This includes removing unsafe tools or implements, providing a limited number of tools to select from, replacing complex tasks with simpler ones that require few or no tools and fewer steps, as well as similar modifications.

Related Disorders

Other movement disturbances may be related to or confused with the limb apraxias. The alien limb phenomenon, mentioned previously as a potential result of callosal lesions, is the experience that a limb feels foreign and has involuntary semipurposeful movements, such as spontaneous limb levitation. This disorder can occur from neurodegenerative conditions, most notably corticobasal syndrome. Akinesia is the inability to initiate a movement in the absence of motor deficits, and hypokinesia is a delay in initiating a response. Akinesia and hypokinesia can be directional, with decreased initiation of movement in a specific spatial direction or hemifield. Akinesia and hypokinesia result from a failure to activate the corticospinal system due to Parkinson disease and diseases that affect the frontal lobe cortex, basal ganglia, and thalamus.

Several other movement disturbances are associated with frontal lobe dysfunction. Motor impersistence is the inability to sustain a movement or posture and occurs with dorsolateral frontal lesions. Magnetic grasp and grope reflexes with automatic reaching for environmental stimuli are primitive release signs. In echopraxia, some patients automatically imitate observed movements. Along with utilization behavior, echopraxia may be part of the environmental dependency syndrome of some patients with frontal lesions. Catalepsy is the maintenance of a body position into which patients are placed (waxy flexibility). Two related terms are mitgehen (“going with”), where patients allow a body part to move in response to light pressure, and mitmachen (“doing with”), where patients allow a body part to be put into any position in response to slight pressure, then return the body part to the original resting position after the examiner releases it. Motor perseveration is the inability to stop a movement or a series of movements after the task is complete. In recurrent motor perseveration, the patient keeps returning to a prior completed motor program, and in afferent or continuous motor perseveration, the patient cannot end a motor program that has just been completed.

Summary

Limb apraxia, or the disturbance of learned skilled movements, is an important but often missed or unrecognized impairment. Clinicians may misattribute limb apraxia to weakness, hemiparesis, clumsiness, or other motor or cognitive disturbance. Apraxia may only be evident in natural or real situations, with actual tool or object use, or on fine, sequential, or specific movements of the upper extremities (Zadikoff and Lang, 2005). Apraxia is an important cognitive disturbance and a salient sign in patients with strokes, Alzheimer disease, corticobasal syndrome, and other conditions. The model of left parietal movement formulas and disconnection syndromes introduced by Liepmann over 100 years ago continues to be compelling today. This model, in the context of a dedicated apraxia examination and analysis for spatiotemporal or content errors, clarifies and classifies the limb apraxias. Although more effective treatments need to be developed, rehabilitation strategies can be helpful interventions for these disturbances. Fortunately, recent advances in technology and rehabilitation promise to enhance our understanding and management of the limb apraxias.

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