Limb Apraxias and Related Disorders PDF

11 Limb Apraxias and Related Disorders Mario F. Mendez, Leila Parand OUTLINE Historical Perspective, 121 Testing for Ideomotor Apraxia, Parietal and Disconnection A Model for Praxis, 121...

11 Limb Apraxias and Related Disorders Mario F. Mendez, Leila Parand OUTLINE Historical Perspective, 121 Testing for Ideomotor Apraxia, Parietal and Disconnection A Model for Praxis, 121 Variants, 124 Classification of Limb Apraxias, 122 Testing for Dissociation Apraxia, 124 Ideomotor Apraxia, Parietal Variant, 122 Testing for Ideational Apraxia, 124 Ideomotor Apraxia, Disconnection Variant, 122 Testing for Conceptual Apraxia, 125 Dissociation Apraxia, 122 Testing for Limb-Kinetic Apraxia, 125 Ideational Apraxia, 122 Testing for Callosal Apraxia, 125 Conceptual Apraxia, 123 Pathophysiology of Limb Apraxias, 125 Limb-Kinetic Apraxia, 123 Rehabilitation for Limb Apraxias, 126 Callosal Apraxia, 123 Related Disorders, 126 Testing for Limb Apraxias, 123 Summary, 126 Apraxia is an inability to correctly perform learned skilled movements. Limb apraxia often results in major functional impairment, even In limb apraxias, there is an inability to correctly execute these move- when subtle, as it affects critical movements of the arms, hands, and ments in an arm or hand owing to neurological dysfunction. Apraxia fingers. Limb apraxia correlates with greater caregiver dependence is essentially a cognitive deficit in motor programming and results in and need for help with activities of daily living (ADLs) (Smania et al., errors either of the spatiotemporal processing of the movements or in 2006), and it can also interfere with rehabilitation therapy and the use the content of the actions. During the course of an apraxia examina- of gestural communication. tion, these errors can help distinguish the major types of limb apraxias. Despite its importance, clinicians often fail to recognize limb A first step in recognizing the limb apraxias is distinguishing them apraxia. In many left hemisphere strokes, right hemiparesis masks the from other causes of impaired movement. First, apraxia is distinct presence of right limb apraxia, and the assumption of normal clum- from elementary motor deficits such as weakness, hemiparesis, spas- siness of the nondominant hand may mask the presence of left limb ticity, ataxia, or extrapyramidal disturbances. Second, apraxia is distin- apraxia. Patients with limb apraxia from left hemisphere strokes can guishable from impaired movements due to primary sensory deficits, have a reduced awareness of limb apraxia (Kusch et al., 2018), making hemispatial neglect, spatial or object agnosia, or other sensory or spa- recovery more difficult. Even when there are no masking factors, the tial disorders. Third, apraxia is distinct from abnormal movements or presence of limb apraxia may still go undetected. Many examiners do postures such as tremor, myoclonus, choreoathetosis, or dystonic pos- not evaluate patients for limb apraxia, do not know how to test for turing. Finally, it is not apraxia if the impaired movements result from apraxia, or cannot recognize the spatiotemporal or content errors pro- other cognitive disorders involving attention, memory, language com- duced by this condition. prehension, or executive functions (Leiguarda and Marsden, 2000). This chapter is about the limb apraxias. The term apraxia occurs Limb apraxia is not rare or insignificant. Apraxia occurs in about broadly in neurology and is usually interchangeable with dyspraxia. 50%–80% of patients with left hemisphere lesions and can persist as a Clinicians use apraxia to describe nonlearned motor dysfunctions chronic deficit in 40%–50% of these. It occurs in a variety of disorders, including oculomotor movements, gait initiation (magnetic apraxia), including stroke (Donkervoort et al., 2000), multiple sclerosis (Kamm and eyelid opening. They also use apraxia to describe skilled motor et al., 2012, Rapaić et al., 2014), tumors such as parietal gliomas tasks that are dependent on visuospatial processing, including optic, (Liouta et al., 2018), corticobasal syndrome (Armstrong et al., 2013), constructional, and dressing apraxia. Apraxia correctly applies to con- Alzheimer disease (Stamenova et al., 2014), some forms of primary ditions that are more clearly consistent with the definition of distur- progressive aphasia (Adeli et al., 2013), Parkinson disease, demen- bances in learned skilled movements but involve body parts other than tia with Lewy bodies (Nagahama et al., 2015), Huntington disease the limbs, including oro-buccal-facial and speech apraxias. These clin- (Zadikoff and Lang, 2005), Creutzfeldt-Jakob disease (Gonzales and ical entities are not included in this chapter, because they are either not Soble, 2017), and even some patients with schizophrenia (Dutschke limb apraxias or not true disorders of “praxis” in the sense of distur- et al., 2018, Stegmayer et al., 2016). A careful examination for limb bances in learned skilled movements (Zadikoff and Lang, 2005). The apraxia can lead to the differentiation of diseases such as Alzheimer focus of this chapter is on the seven major limb apraxias of the upper disease from frontotemporal dementia, or dementia with Lewy bodies extremities. They include ideomotor apraxia, parietal variant; ideo- from other disorders (Ahmed et al., 2016; Nagahama et al., 2015). motor apraxia, disconnection variant; dissociation apraxia; ideational 120 @ @ @ D D D D @ D1 F CD @ 2C @ C C@ @ ). @ 4 C F  CHAPTER 11 Limb Apraxias and Related Disorders 121 apraxia; and conceptual apraxia. Also included is limb-kinetic apraxia, Visual input Action semantics Verbal input a disorder that some argue is not a true apraxia, but instead a more (posterior parietal) basic disturbance in fine motor movements. Callosal apraxias com- prise a separate category because of their unique unilateral and varied manifestations. Movement Verbal formulas semantics HISTORICAL PERSPECTIVE (left parietal lobe) Many clinicians and investigators helped develop the current concept of limb apraxia. In 1866, John Hughlings Jackson probably recognized limb apraxia when he observed that the patient had “power in his muscles and in the centres for coordination of muscular groups, but Motor programs Motor programs he—the whole man, or the ‘will’—cannot set them agoing” (Pearce, (left supplementary (right supplementary motor area) Via corpus motor area) 2009). In 1870, Carl Maria Finkelnburg used “asymbolia” to describe callosum 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 “paraki- Left corticospinal Right corticospinal system system nesia” to describe a patient who “though retaining the concepts for (left primary (right primary her actions, did not succeed in awakening the corresponding kinetic motor cortex) motor cortex) image.” By this time, the stage was set for Hugo Karl Liepmann’s sem- inal model of the limb apraxias. In the early 1900s, Liepmann published a series of papers that Right limb output Left limb output led to the contemporary concept of limb apraxias. He proposed that the execution of purposeful movements could be divided into three Fig. 11.1 A Model of Praxis. 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 associa- information, and general principles of tool use (Goldenberg and Spatt, tion of these movement formulas via cortical connections with the 2009; Ochipa et al., 1992). “innervatory patterns” or motor programs located in the left “sen- If a movement involves the use of a tool or object, action seman- somotorium” (which includes premotor and supplementary motor tics specify knowledge of tool action (turning, pounding, etc.) and the areas [SMAs]). Third is the transmission of the information to the knowledge of which tool or object to use for a task (Leiguarda and left primary motor cortex for performance of the intended actions Marsden, 2000). in the right limb. Finally, in order for the left limb to perform the Beyond movement formulas and action semantics, a third import- movements, the information traverses the corpus callosum to the ant element of models of praxis is the motor programs themselves. right sensomotorium to activate the right primary motor cortex. In the premotor region, the SMA translates the movement formulas Using Heymann Steinthal’s term of “apraxia,” Liepmann classi- into motor programs before sending them on to primary motor cor- fied disturbances in these connections as “ideational, ideo-kinetic tex (Roy and Square, 1985). The SMA, which is involved in sequen- (melokinetic), and limb-kinetic apraxia.” Over the years, this classi- tial movements and bimanual coordination of the upper extremities, fication nomenclature has evolved and the application of these terms receives projections from parietal neurons and in turn projects axons has shifted, but Liepmann’s basic formulation of apraxia has per- to motor neurons in the primary motor cortex. The SMA translates the sisted to the present day. parietal 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 A MODEL FOR PRAXIS in the ipsilateral extremity, the brain further conveys these programs Models of apraxia emerge from this historical perspective. Most models across the corpus callosum to the opposite premotor cortex. of praxis include a left parietal hub with connections to anterior motor Beyond this traditional model for praxis, apraxia may result from areas with a central role of learning and converting mental images of damage in other regions including the prefrontal cortex, right hemi- intended action into motor execution (Heilman and Rothi, 2012) (Fig. sphere, basal ganglia (putamen and globus pallidus), thalamus, and 11.1). These spatiotemporal movement formulas, also known as prax- their white-matter connections. icons or visuokinesthetic motor engrams, are necessary for learned The prefrontal region participates in sequencing multiple arm, skilled movements. Multiple input modalities including visual, ver- hand, and finger movements. Functional magnetic resonance imaging bal-auditory, and tactile can activate these movement formulas. Cells studies suggest that proximal limb control representations are associ- in the inferior parietal lobule fire selectively in response to hand move- ated with bilateral inferior frontal gyri for both limbs, while distal limb ments, visually presented information about object size and shape, or control areas generally left lateralized for both limbs (Mäki-Marttunen the actual manipulation of objects, and functional neuroimaging stud- et al., 2014). Both parietal regions participate in the integration of ies show activity of this region in response to recognition of actions visual information and upper-extremity movement, and in perform- associated with object or tool use (transitive actions) (Damasio et al., ing nonpurposeful movements—a necessary aspect for learning new 2001). Functional neuroimaging studies have also shown activity in purposeful movements. Although the left inferior parietal lobule is left parietal sub-regions with privileged connectivity to premotor and more active than the right during action imagery and actual discrim- sensory areas (Garcea and Mahon, 2014). In addition to movement ination of nonpurposeful gestures, the right parietal region is more formulas, the left parietal region appears to contain action semantics active during imitation and when these gestures consist of finger pos- and conceptual systems such as tool action, tool–object association tures (Buccino et al., 2001; Hermsdorfer et al., 2001). @ @ @ D D D D @ D1 F CD @ 2C @ C C@ @ ). @ 4 C F 122 PART I Common Neurological Problems The role of basal ganglia and thalamus is less clear, but they function E as part of cortical–subcortical motor loops. Apraxia could, theoreti- D Visual input Action semantics Verbal input cally, result from damage to any of these areas outside the traditional (posterior parietal) model of praxis. C D E Newer models of praxis have focused on network activation as A opposed to isolated regional activation. The posterior left parietal and Movement C Verbal temporal cortices as well as the dorsolateral prefrontal cortex are acti- formulas semantics vated when hand gestures are planned and executed. This left pari- (left parietal lobe) eto-fronto-temporal network, or “praxis representation network” (Króliczak and Frey, 2009; Roy et al., 2014), includes two main streams: B a ventral stream that processes semantic knowledge (the “what” path- way) and a dorsal stream that processes spatiotemporal information Motor programs Motor programs (the “where” pathway) (Brandi et al., 2014). Abnormalities of the G (left supplementary (right supplementary ventral stream may impair action semantics such as the retrieval of motor area) Via corpus motor area) tool-action concepts (Hoeren et al., 2014), and abnormalities of the callosum B B B B dorsal pathway may result in spatiotemporal errors in executing move- ment formulas (Martin et al., 2017). The left supramarginal gyrus and Left corticospinal Right corticospinal left caudal middle temporal gyrus contribute to the integration of con- system system cepts with motor representations into actions (Króliczak et al., 2016). (left primary (right primary Consistent with a left parieto-fronto-temporal network, damage in the motor cortex) motor cortex) inferior frontal cortex reaching to the temporal pole is associated with F F an increased frequency of Body-Part-as-Object errors on praxis testing (Finkel et al., 2018). Right limb output Left limb output This left parieto-fronto-temporal praxis network significantly over- laps with the mirror neuron network for understanding the intentional Fig. 11.2 Lesions in Limb Apraxias. Praxis disturbances can result actions of others (Cattaneo, 2009). Left hemisphere stroke patients from various brain localizations as illustrated here. A, Ideomotor apraxia, parietal variant. B, Ideomotor apraxia, disconnection variant. C, Ver- with apraxia with deficits in gesture comprehension have had lesions bal dissociation apraxia. D, Visual dissociation apraxia. E, Conceptual in more anterior parts of the mirror neuron system, whereas those apraxia. F, Limb-kinetic apraxia. G, Callosal apraxia. with gesture imitation deficits have had lesions in more posterior parts (Binder et al., 2017). programs in the SMA or in their intra- and interhemispheric connec- tions (Heilman and Watson, 2008). These lesions result in impaired CLASSIFICATION OF LIMB APRAXIAS pantomime to verbal commands, impaired imitation of gestures, and Beginning with Liepmann, there have been multiple attempts to clas- the presence of spatiotemporal production errors. The movement for- sify and define the limb apraxias (Hanna-Pladdy and Rothi, 2001). The mulas themselves are preserved and, in contrast to the parietal variant classification presented here is based on the seminal work of Heilman of ideomotor apraxia, these patients can recognize and identify ges- and associates, who have significantly contributed to the understand- tures. The lesions lie along the route from the left inferior parietal cor- ing of the limb apraxias (Heilman and Rothi, 2012). Depending on tex to primary motor cortices (see Fig. 11.2, B). Although SMA lesions the location of the lesion, the patient has different patterns of ability tend to affect both upper extremities, if the SMA lesion is limited to the to imitate and recognize gestures, perform sequential movements, and right, apraxia may be limited to the left upper extremity. do fine motor activities (Fig. 11.2). The presence of production and content errors further characterizes the subtypes of limb apraxia. Dissociation Apraxia Patients with dissociation apraxia only exhibit errors when the move- Ideomotor Apraxia, Parietal Variant ment is evoked by stimuli in one specific modality, usually the verbal The parietal variant of ideomotor apraxia may be the most common or language modality. Dissociation apraxia is usually a specific dis- and prototypical limb apraxia. Disruption of the movement formulas connection between language areas and movement formulas in the in the inferior parietal lobule impairs skilled movements on command inferior parietal lobule. However, information can reach the inferior and to imitation, as well as the recognition of gestures (see Fig. 11.2, parietal lobe via input modalities other than language. Patients with A). Patients make spatial and temporal errors while producing move- dissociation apraxia may be impaired when attempting to perform ments. There is a failure to adopt the correct posture or orientation skilled movements in response to verbal commands, but they are able of the arm and hand or to move the limb correctly in space and at the to imitate gestures and to indicate or use actual objects correctly. An correct speeds. Spatial errors involve the configuration of the hand and important distinguishing feature of dissociation apraxia is errors that fingers, the proper orientation of the limb to the tool or object, and the are often unrecognizable movements, rather than the spatiotemporal spatial trajectory of the motion. A major distinguishing feature of the or content errors of other apraxia syndromes. In addition to verbal parietal variant of ideomotor apraxia is difficulty recognizing or iden- dissociation apraxia (see Fig. 11.2, C), there can be visual (see Fig. 11.2, tifying gestures, implicating damage to the praxicons, visuokinesthetic D) and tactile dissociation apraxias as well. motor engrams, or movement formulas themselves. Ideational Apraxia Ideomotor Apraxia, Disconnection Variant Ideational apraxia is the inability to correctly order or sequence a This form of ideomotor apraxia is a disconnection of an intact parietal series of movements to achieve a goal. It is a disturbance in an over- region from the pathways to primary motor cortices. The disconnec- all ideational action plan. When these patients are given components tion variant of ideomotor apraxia results from disruptions of motor necessary to complete a multistep task, they have trouble carrying out @ @ @ D D D D @ D1 F CD @ 2C @ C C@ @ ). @ 4 C F  CHAPTER 11 Limb Apraxias and Related Disorders 123 the steps in the proper order, such as preparing, addressing, and then individuals, or they may have a similar lateralization as right-handers. mailing a letter. However, the individual steps are performed accu- Liepmann and others described left-sided disconnection-variant rately. The lesions responsible for ideational apraxias are not clear; the ideomotor apraxia due to callosal lesions and strokes (Heilman and deficits usually occur in patients with diffuse cerebral processes such Watson, 2008). These patients cannot pantomime with their left hand as dementia, delirium, or extensive lesions in the left hemisphere that to verbal command or imitate but can recognize and identify gestures. involve the frontal lobe and SMA. Unfortunately, use of the term ide- Others described left-sided dissociative apraxia due to callosal lesions ational apraxia has been confusing, with the term erroneously applied (Gazzaniga et al., 1967; Geschwind and Kaplan, 1962). Patients who to conceptual apraxia and other disorders. Ideational apraxia is not a have had surgical disconnection of the corpus callosum could not ges- conceptual problem in the proper application or use of tools or objects, ture normally to command with their left arm and hand but performed but rather a problem in sequencing of actions in multistep behaviors. well with imitation and actual tools. Some patients have had a com- bination of both disconnection-variant ideomotor and dissociative Conceptual Apraxia apraxia of their left arm and hand manifested by unrecognizable move- Conceptual apraxia results in errors in action semantics, specifically ments on verbal command and spatiotemporal errors on imitation. involving the content of the action, such as in tool-selection errors or There is also the possibility of developing both limb-kinetic apraxia in tool–object knowledge. Whereas dysfunction of praxis production and ideomotor apraxia in the left hand with focal mesial lesions of the results in ideomotor apraxia, defects in the conceptual knowledge corpus callosum (Acosta et al., 2014). needed to successfully select tools and objects results in conceptual Other patients have a callosal “alien limb” with independent apraxia. Although conceptual apraxia often co-occurs with ideomotor movements of the nondominant limb, sometimes with “diagonistic apraxia, it can occur by itself, indicating that praxis production and apraxia,” or the intermanual conflict of the hands acting in opposi- praxis conceptual systems are independent. Patients with conceptual tion to each other. The classic example of this is the split-brain patient apraxia are unable to name or point to a tool when its function is dis- who has undergone a corpus callosotomy and finds that his or her left cussed, or recall the type of actions associated with specific tools, uten- hand is unbuttoning his shirt or blouse while the right one is trying to sils, or objects. They make content errors in which they substitute the button it. Finally, there is a rare description of callosal lesions resulting action associated with the wrong tool for the requested tool. For exam- in conceptual apraxia, indicating that conceptual knowledge as well ple, when asked to demonstrate the use of a hammer or a saw either by as movement formulas have lateralized representations, and that such pantomiming or using the tool, the patient with the loss of tool–object representations are contralateral to the preferred hand (Heilman et al., action knowledge may pantomime a screwing twisting movement as if 1997). using a screwdriver. Other terms used to describe these errors include disturbances in mechanical knowledge or in action semantics (see Fig. 11.2, E). Conceptual apraxia is most common in Alzheimer disease, TESTING FOR LIMB APRAXIAS in other dementias (Ochipa et al., 1992), and in patients with diffuse Apraxia testing requires a systematic approach (Box 11.1). Prior to posterior cerebral lesions, particularly involving the left hemisphere. testing of praxis, a neurological examination excludes the presence of significant motor, sensory, or cognitive disorders that could explain Limb-Kinetic Apraxia the inability to perform learned skilled movements. First, the testing Limb-kinetic apraxia results from disturbed motor programs. These of praxis itself begins with asking the patient to pantomime to com- patients have an inability to make finely graded, precise, coordinated mand. The movements are transitive (associated with tool or instru- individual finger movements. Limb-kinetic apraxia is not an apraxia in ment use) and intransitive (associated with communicative gestures the traditional definition, but it is prominently considered in the dif- such as waving goodbye). For transitive movements, the examiner ferential diagnosis of the limb apraxias, and, therefore, discussed here. asks patients to demonstrate how to comb their hair, brush their teeth, Patients with limb-kinetic apraxia complain of a loss of dexterity or or use a pair of scissors. For intransitive movements, the examiner deftness that makes fine motor movements such as buttoning or tying asks patients to demonstrate how to wave goodbye, beckon some- shoes difficult. Weakness or changes in muscle tone do not account body to come, or hitchhike. The testing involves the right and left for this “clumsiness,” and limb-kinetic apraxia may be intermediate limbs independently. The examiner observes the patients’ responses between paresis and other limb apraxias. Limb-kinetic apraxia is usu- for the presence of temporal-spatial or content errors. Second, if ally confined to the limb contralateral to a hemispheric lesion; how- patients have difficulty pantomiming movements, the examiner tests ever, when limb-kinetic apraxia occurs in the preferred hand, it may their ability to imitate gestures. For gesture imitation, the examiner also be present in the nonpreferred hand (Hanna-Pladdy et al., 2002). performs both transitive and intransitive movements and asks the Clinicians need to distinguish limb-kinetic apraxia from right parietal patient to copy the movements. Gesture imitation should also include functions such as nonsymbolic gestures (e.g., copying meaningless fine meaningless, or nonrepresentational, gestures such as linking pin- finger movements) and from optic ataxia, or decreased coordination kies or interlocking circles made with the thumb and index finger on of the hands under visual guidance. Limb-kinetic apraxia results from each hand. Disturbed meaningless gestures can signify a number of lesions in the left SMA, the primary motor cortex, or even in the corti- conditions including an inability to apprehend spatial relationships cospinal system (see Fig. 11.2, F) (Kubel et al., 2018). Liepmann (1920) involving the hands and arms in parietal-variant ideomotor apraxia, also thought that limb-kinetic apraxia could result from lesions in the a basic disturbance in idiokinetic movements, or abnormalities in sensory motor cortex, and Kleist (1931) attributed it to damage in the spatial processing from the right parietal lobe (Goldenberg, 2013). premotor areas. Imitating meaningless gestures bimanually may be particularly dis- turbed if there is biparietal disease, such as with Alzheimer disease Callosal Apraxia (Sanin and Benke, 2017). Several limb apraxia syndromes can result from callosal lesions (see Third, for gesture knowledge, the examiner performs the same Fig. 11.2, G). What distinguishes these patients is that their apraxia transitive and intransitive gestures and asks the patient to identify is confined to the nondominant limb, usually the left arm or hand in the gesture. The patient must identify the gesture and discriminate right-handed individuals. The right limb may be affected in left-handed between those that are well and those that are poorly performed. @ @ @ D D D D @ D1 F CD @ 2C @ C C@ @ ). @ 4 C F 124 PART I Common Neurological Problems patient’s ability to use real objects usually indicates a marked severity BOX 11.1 The Examination for Limb of the limb apraxia. The pattern of deficits will determine the types of Apraxia apraxia (Table 11.1). Specialists in occupational therapy, physical ther- I. DOMINANT UPPER EXTREMITY apy, speech pathology, and neuropsychology can further assess and 1. PANTOMIME TO VERBAL COMMAND quantify the deficits in limb apraxia using instruments like the Apraxia a. Transitive actions: Battery for Adults-2, the Florida Apraxia Battery, the Cologne Apraxia Comb hair Screening, the Test of Upper Limb Apraxia, Short screening Test for Brush teeth Ideomotor Apraxia (STIMA), Diagnostic Instrument of Limb Apraxia Flip a coin (DILA) and its short version (DILA-S), and others (Buchmann and Use scissors Randerath, 2017; Dovern et al., 2012; Power et al., 2010; Tessari et al., Use a hammer 2015; Vanbellingen et al., 2010). Use a key Use a screwdriver Testing for Ideomotor Apraxia, Parietal and b. Intransitive actions: Disconnection Variants Wave goodbye Patients with the ideomotor apraxias cannot pantomime to command Beckon someone to come or imitate the examiner’s gestures. These patients improve only par- Indicate someone to stop tially with intransitive acts, imitation, and real object use. Ideomotor Salute apraxia results in spatiotemporal errors in the positioning and orien- Show how to hitchhike tation of the arm, hand, and fingers to the target and in the timing Give the peace sign of the movements, but the goal of the action is still recognizable. In Give the OK sign addition to poor positioning of the limb in relation to an imagined 2. IMITATION OF GESTURES object, patients with ideomotor apraxia have an incorrect trajectory of The examiner demonstrates the same actions without naming them and their limb through space owing to poor coordination of multiple joint asks the patient to copy them. movements. Patients with ideomotor apraxia also have hesitant, stut- The examiner also tests the imitation of meaningless gestures such as tered movements rather than smooth, effortless ones. The difference linking pinkies or interlocking circles made with the thumb and index between parietal variant and disconnection types of ideomotor apraxia finger on each hand. is that patients with the disconnection variant can comprehend ges- 3. GESTURE KNOWLEDGE tures and pantomimes and discriminate between correctly and incor- The examiner demonstrates different actions and asks the patient to rectly performed pantomimes. identify their function/purpose and how well they were performed. On attempting to pantomime, patients with ideomotor apraxia 4. SEQUENTIAL ACTIONS may substitute a body part for the tool or object (“Body-Part-as- The examiner asks the patient to show how to prepare a letter for mail- Object” error) (Raymer et al., 1997). For example, when attempting ing, a sandwich for eating, a bowl of cereal with milk. The examiner to pantomime combing their hair or brushing their teeth, they sub- instructs the patient that the imaginary elements needed for the task stitute their fingers for the comb or toothbrush. Normal subjects are laid out in front of them. may make the same errors, so the examiner should ask patients not 5. CONCEPTUAL KNOWLEDGE to substitute their fingers or other body parts but to pantomime The examiner shows the patient either pictures or the actual tools or using a “pretend tool.” Patients with ideomotor apraxia may not objects and asks the patient to pantomime or demonstrate their use improve with these instructions and continue to make Body-Part- or function. The examiner may also show a task, such as holding a as-Object errors. The persistent substitution of a body part for a nail, and ask the patient to pantomime the correct tool use and action. tool or object may indicate a left frontal disturbance. In addition, 6. LIMB-KINETIC MOVEMENTS this type of error activates the right inferior parietal lobe; hence, Finger tapping patients with ideomotor apraxia with left parietal injury may be Alternate touching each fingertip with thumb using their normal right parietal lobe in order to pantomime ges- Pick up a coin without sliding tures (Ohgami et al., 2004). Twirl coin between thumb, index, and middle fingers 7. REAL OBJECT USE Testing for Dissociation Apraxia If limb apraxia is present, test with real object use. Most limb apraxias The testing for dissociation apraxia is the same as for ideomotor improve when using real objects for transitive actions and when ges- apraxia. An important feature of dissociation apraxia when attempt- turing spontaneously with intransitive actions. ing to pantomime is the absence of recognizable movements. When II. NONDOMINANT UPPER EXTREMITY asked to pantomime to verbal command, these patients may look at The examiner repeats the same procedures as for the dominant upper their hands but fail to perform any pertinent actions. However, unlike extremity. patients with ideomotor apraxia, they can imitate the examiner’s actions. Given the language–motor disconnection, it is important to evaluate the patient for language disorders and to exclude aphasia. Fourth, the patient must perform tasks that require several motor Similar defects in other modalities are possible as well. For example, acts in sequence, such as making a sandwich or preparing a letter for some patients who are asked to pantomime in response to visual or mailing. Fifth, the examiner shows the patient pictures of tools or tactile stimuli may be unable to do so but can correctly pantomime to objects or the actual tools or objects themselves. The examiner then verbal command. requests that the patient pantomime the action associated with the tool or object. Finally, the examiner checks for fine finger movements Testing for Ideational Apraxia by asking the patient to do repetitive tapping, picking up a coin with The test for ideational apraxia involves pantomiming multistep a pincer grasp, and twirling the coin. Additional impairment in the sequential tasks to verbal command. Examples are asking the patient @ @ @ D D D D @ D1 F CD @ 2C @ C C@ @ ). @ 4 C F  CHAPTER 11 Limb Apraxias and Related Disorders 125 TABLE 11.1 Testing in Limb Apraxias Ideomotor, Ideomotor, parietal disconnection* Dissociation* Ideational* Conceptual* Limb-kinetic Pantomime to Abnormal† Abnormal† Abnormal‡ Normal§ Abnormal‖ Normal verbal command Imitation of Abnormal† Abnormal† Normal Normal§ Normal Normal¶ gestures Gesture knowledge Abnormal Normal Normal Normal Normal Normal Sequential actions Normal† Normal Abnormal Abnormal Abnormal Normal Conceptual knowl- Normal Normal Normal Abnormal/normal§ Abnormal Normal edge of tool use Limb-kinetic Normal Normal Normal Normal Normal Abnormal movement Real object use Normal/abnormal# Normal/abnormal# Normal Normal/abnormal# Abnormal‖ Normal/abnormal# *Callosal apraxia, which is limited to the nondominant limb, can present as disconnection-variant ideomotor apraxia, a dissociative apraxia, or (rarely) a conceptual apraxia. †Spatiotemporal production errors on single, individual ideomotor tasks. ‡Unrecognizable movements or attempts. §Errors on performing sequential actions only (i.e., individual actions and their conceptual knowledge are normal). ‖Content and tool use errors on individual ideomotor tasks. ¶Decreased dexterity in fine finger movements. #Errors depend on severity. In general, errors are worse with verbal commands>imitation>real spontaneous object use and worse for transitive rather than intransitive actions. to demonstrate how to prepare a letter for mailing or a sandwich for hand. The testing for callosal apraxia may reveal a disconnection-vari- eating. The examiner instructs the patient that the imaginary elements ant ideomotor apraxia, a dissociative apraxia, or even a conceptual needed for the task are laid out in front of them; the patient is then apraxia in the nondominant limb (Heilman et al., 1997). observed to see whether the correct sequence of events is performed. Ideational apraxia manifests as a failure to perform each step in the correct order. If disturbed, the examiner can repeat this testing with a PATHOPHYSIOLOGY OF LIMB APRAXIAS real object, such as providing the patient with a letter and stamp. Ideomotor apraxia is associated with left hemispheric lesions in a variety of structures including the inferior parietal lobe, the frontal Testing for Conceptual Apraxia lobe, and the premotor areas, particularly the SMA. There are reports Patients with conceptual apraxia make content errors and demonstrate of ideomotor apraxia due to subcortical lesions in the basal ganglia the actions of tools or objects other than the one they were asked to (caudate-putamen), thalamus (pulvinar), and associated white-mat- pantomime. For example, the examiner shows the patient either pic- ter tracts including the corpus callosum. Limb apraxias can be caused tures or the actual tools or objects and asks the patient to pantomime by any central nervous system disorder that affects these regions. The or demonstrate their use or function. Patients with conceptual apraxia different forms of limb apraxia result from cerebrovascular lesions, pantomime the wrong use or function, but they are able to imitate ges- especially left middle cerebral artery strokes with right hemiparesis tures without spatiotemporal errors (see Table 11.1). and apraxia evident in the left upper extremity. Right anterior cere- bral artery strokes and paramedian lesions could produce ideomotor Testing for Limb-Kinetic Apraxia apraxia, disconnection variant. Ideomotor apraxia and limb-kinetic For limb-kinetic apraxia testing, the examiner asks the patient to per- apraxia can be the initial or presenting manifestation of disorders form fine finger movements and looks for evidence of incoordination. such as corticobasal syndrome, primary progressive aphasia, pari- For example, the examiner asks the patient to pick up a small coin such etal-variant Alzheimer disease, and other disorders (Rohrer et al., as a dime from the table with the thumb and the index finger only. 2010). Normally, people use the pincer grasp to pick up a dime by putting a There are important considerations of hemispheric specialization forefinger on one edge of the coin and the thumb on the opposite edge. and handedness on praxis. Early investigators proposed that handed- Patients with limb-kinetic apraxia will have trouble doing this with- ness was related to the hemispheric laterality of the movement for- out sliding the coin to the edge of the table or using multiple fingers. mulas. Studies using functional imaging have provided converging Another test involves the patient rotating a nickel between the thumb, evidence that in people who are right-handed, it is the left inferior index, and middle fingers 10 times as rapidly as they can. Patients with parietal lobe that appears to store the movement formulas needed limb-kinetic apraxia are slow and clumsy at these tasks (Hanna-Pladdy for learned skilled movements (Muhlau et al., 2005). However, left- et al., 2002). In addition, they may also have disproportionate prob- handed people may demonstrate an ideomotor apraxia from a right lems with meaningless gestures. These tasks, particularly the simple hemisphere lesion, because their movement formulas can be stored in coin rotation test, provide valuable information about dexterity skills their right hemisphere. It is not unusual to see right-handed patients for ADLs (Foki et al., 2016). with large left hemisphere lesions who are not apraxic, and there are rare reports of right-handed patients with right hemisphere lesions Testing for Callosal Apraxia and limb apraxia (Schell et al., 2014). These findings suggest that hand The examination for callosal apraxias is the same as for the other limb preference is not entirely determined by the laterality of the movement apraxias except that the abnormalities are limited to the nondominant formulas, and praxis and handedness can be dissociated. @ @ @ D D D D @ D1 F CD @ 2C @ C C@ @ ). @ 4 C F 126 PART I Common Neurological Problems REHABILITATION FOR LIMB APRAXIAS RELATED DISORDERS Because many instrumental and routine ADLs depend on learned Other movement disturbances may be related to or confused with the skilled movements, patients with limb apraxia usually have impaired limb apraxias. The alien limb phenomenon, a potential result of callo- functional abilities. The presence of limb apraxia, more than any other sal lesions, is the experience that a limb feels foreign and has involun- neuropsychological disorder, correlates with the level of caregiver tary semipurposeful movements, such as spontaneous limb levitation. assistance required 6 months after a stroke, whereas the absence of This disorder can occur from neurodegenerative conditions, most apraxia is a significant predictor of return to work after a stroke (Saeki notably corticobasal syndrome. Akinesia is the inability to initiate a et al., 1995). The treatment of limb apraxia is therefore important for movement in the absence of motor deficits, and hypokinesia is a delay improving the quality of life of the patient. in initiating a response. Akinesia and hypokinesia can be directional, Even though many apraxia treatments have been studied, none with decreased initiation of movement in a specific spatial direction or has emerged as the standard. There are no effective pharmacothera- hemifield. Akinesia and hypokinesia result from a failure to activate pies for limb apraxia, and treatments primarily involve rehabilitation the corticospinal system due to Parkinson disease and diseases that strategies. Buxbaum and associates (2008) surveyed the literature on affect the frontal lobe cortex, basal ganglia, or thalamus. the rehabilitation of limb apraxia and identified 10 studies with 10 Several other movement disturbances are associated with frontal lobe treatment strategies: multiple cues, error type reduction, six-stage task dysfunction. Motor impersistence is the inability to sustain a movement hierarchy, conductive education, strategy training, transitive/intran- or posture and occurs with dorsolateral frontal lesions. Magnetic grasp sitive gesture training, rehabilitative treatment, error completion, and grope reflexes with automatic reaching for environmental stimuli are exploration training, and combined error completion and exploration primitive release signs. In echopraxia, some patients automatically imitate training. Most of these approaches emphasize cueing with multiple observed movements. Along with utilization behavior, echopraxia may modalities, with verbal, visual, and tactile inputs, repetitive learn- be part of the environmental dependency syndrome of some patients ing, and feedback and correction of errors. If possible, rehabilitation with frontal lesions. Catalepsy is the maintenance of a body position into techniques should involve activities that are akin to a natural setting which patients are placed (waxy flexibility). Two related terms are mitge- (Baak et al., 2015). The timing of rehabilitation may be an important hen (“going with”), where patients allow a body part to move in response factor as well. Apraxia patients with acute lesions, such as left hemi- to light pressure, and mitmachen (“doing with”), where patients allow sphere strokes, appear to respond better if the therapy is initiated early a body part to be put into any position in response to slight pressure, (Mutha et al., 2017). Patients with post-stroke apraxia have had gener- then return the body part to the original resting position after the exam- alization of cognitive strategy training to other ADLs (Geusgens et al., iner releases it. Motor perseveration is the inability to stop a movement 2006), but, unfortunately, many others have not (Bickerton et al., or a series of movements after the task is complete. In recurrent motor 2006; Shimizu and Tanemura, 2017). Newer technologies such as tran- perseveration, the patient keeps returning to a prior completed motor scranial stimulation of left parietal cortex or primary motor cortex, program, and in afferent or continuous motor perseveration, the patient can temporarily improve praxis in some patients (Bianchi et al., 2015; cannot end a motor program that has just been completed. Bolognini et al., 2015; Park 2018). Other novel techniques for apraxia rehabilitation include embedding sensors in household tools in order to guide rehabilitation (Hughes et al., 2013), using a videogame-based SUMMARY feedback system to improve pinch and grasp forces (Fusco et al., 2018), Limb apraxia, or the disturbance of learned skilled movements, is an and evaluating apraxia with a virtual partner (Candidi et al., 2017). important but often missed or unrecognized impairment. Clinicians may In summary, patients can learn and produce new gestures, and misattribute limb apraxia to weakness, hemiparesis, clumsiness, or other new technologies, including transcranial stimulation, may play a motor, sensory, spatial, or cognitive disturbance. Apraxia may only be evi- role in rehabilitation, but the re-learned specific movements may dent on fine, sequential, or specific movements of the upper extremities not persist or generalize well to contexts outside the rehabilitation and requires a systematic praxis examination (Zadikoff and Lang, 2005). setting. Apraxia is an important cognitive disturbance and a salient sign in patients Nevertheless, some patients with ideomotor apraxia have improved with strokes, Alzheimer disease, corticobasal syndrome, and other condi- with gesture-production exercises (Smania et al., 2000), with positive tions. The model of left parietal movement formulas and disconnection effects lasting 2 months after completion of gesture training (Smania syndromes introduced by Liepmann over 100 years ago continues to be et al., 2006). Patients with apraxia would benefit from referral to a reha- compelling today. This model, in the context of a dedicated apraxia exam- bilitation specialist with experience in treating apraxias (Cantagallo ination and analysis for spatiotemporal or content errors, clarifies and et al., 2012; Dovern et al., 2012). classifies the limb apraxias. Although more effective treatments need to be Additional practical interventions for the management of limb developed, rehabilitation strategies can be helpful interventions for these apraxias involve making environmental changes. This includes disturbances. Fortunately, recent advances in technology and rehabilitation removing unsafe tools or implements, providing a limited num- continue to enhance our understanding and management of limb apraxias. ber of tools to select from, replacing complex tasks with simpler ones that require few or no tools and fewer steps, as well as similar The complete reference list is available online at https://expertconsult. modifications. inkling.com/. @ @ @ D D D D @ D1 F CD @ 2C @ C C@ @ ). @ 4 C F