Ideomotor Apraxia - Selma Greffou

Ideomotor apraxia : A neuroetiological perspective

Presented by: Selma Greffou To: Dr. Julien Doyon Course: neuropsychopathologie (PSY 6413)

Due on March the 13th, 2008 Université de Montréal.

Apraxia Apraxia is a disorder of the execution of actions implicating learned, voluntary and intentional gestures. It is a gesture pathology that cannot be attributable to sensori-motor deficits, comprehension problems, lack of cooperation, or to an important mental deterioration (personal communication: Dr. Bernadette Ska, 2008). Ideomotor apraxia (IMA) is a neurological disorder characterized by the inability to pantomime, imitate, and use tools properly (e.g., comb one’s hair). The movements are spatially incorrect, and may be abnormally slow and deliberate. This deficit may extend into communicative gestures as well (e.g., waving goodbye), but is more often seen in tool-use pantomime. The deficits commonly include orientation errors (e.g., holding a comb upside down on top of the head) and spatial and temporal errors (e.g., carving a turkey with jerky vertical movements instead of smooth anterior– posterior movements). Other deficits include movement errors (e.g., patients make extra and unnecessary movements or move the wrong joints). The use of an object or tool in real-life situations may also be impaired and patients may perform “body part as object” errors (e.g., when instructed to cut a slice of bread, they will use the hand as if it were a knife instead of holding a knife). Moreover, patients with IMA display an automatic-voluntary dissociation: the ability to spontaneously use tools, such as brushing one's teeth in the morning without being instructed to do so, may remain intact but are often lost as well. The classification of the various IMA subtypes are not well defined at present (Wheaton & Hallett, 2007). The general concept of apraxia and the classification of ideomotor apraxia were developed in Germany in the late 19th and early 20th centuries mainly by the work of Hugo Liepmann (Goldberg, 2003). Theories of IMA Many hypotheses have been proposed to explain IMA, amongst them lie the following: 1) difficulties in the activation of the motor patterns corresponding to the representation of the target

gesture (Liepman, 1908); 2) an inability to plan and program more or less complex actions (Hécaen, 1972; Poeck, 1983); 3) a gesture production deficit (Rothi, 1991) whereas conception is intact; 4) a rupture between the idea of the gesture and the execution command; and 5) biological theories which advocate the role of brain lesions in inducing IMA (personal communication: Dr. Bernadette Ska, 2008). Some of the biological theories shall be explored in this paper Pathophysiology of IMA The prevailing hypothesis for the pathophysiology of IMA is that the various brain lesions associated with the disorder disrupt portions of the praxis system. The praxis system is the brain regions that are involved in taking processed sensory input, accessing of stored information about tools and gestures, and translating these into a motor output (Wheaton et al., 2007). Buxbaum et al. (2000) have proposed that the praxis system involves three distinct parts: 1) stored gesture representations, 2) stored tool knowledge, and 3) a dynamic body schema. The first two parts store information about the representation of gestures in the brain and the characteristic movements of tools. The body schema (the 3rd part) is the brain’s model of the body and its position in space. The praxis system relates the stored information about a movement type to how the dynamic and changing body representation varies as the movement progresses. It is still not clear how this system maps out onto the brain itself, although some research has given indications to possible locations for certain portions. The dynamic body schema has been suggested to be localized in the superior posterior parietal cortex. There is also evidence that the inferior parietal lobule may be the locus for storage of the characteristic movements of a tool. If the connections between these areas become severed, the praxis system would be disrupted, possibly resulting in IMA (Buxbaum et al., 2000). In fact, evidence from lesion studies support the model of a praxis system located in the parietal cortex (see next section). Neuroetiology of IMA

The most common cause of IMA is a unilateral ischemic lesion to the brain, which is damage to one hemisphere of the brain due to a disruption of the blood supply, as in a stroke. The lesion brain sites most associated with IMA are the left parietal and premotor areas. It is clear that left-sided parietal lesions commonly produce bilateral deficits on pantomiming tool-use movements and produce more severe deficits of cognitive motor behavior. Makuuchi et al. (2005) claimed that although many studies have identified the left parietal lobe as being the neural correlate for ideomotor praxis (IP), this still remains subject to debate as a study of a large sample claimed a crucial role for deep parietofrontal and occipitofrontal fibres in producing ideomotor apraxia which challenged the traditional view (Kertesz & Ferro 1984). Thus, their objective was to localize the neural substrates of IP using functional magnetic resonance imaging. Brain regions activated by both imitation and verbal command movements were tested against a simple self-paced movement. They tested 22 young, right handed, healthy subjects (20 men, 2 women) from whom functional and anatomical data were collected during praxis. The experiment comprised three motor conditions (imitation, movements executed by verbal command, and finger bending/unbending) and a rest condition. All motor tasks were performed using the left hand (because the right hand is often paralyzed in patients with apraxia). Imitation stimuli consisted of 18 drawings of left hand postures and identical postures were instructed verbally for the verbal command condition. The finger bending/unbending movement was self-paced. Blood oxygenation level dependent (BOLD) signal increases were compared during two kinds of IP (imitation and verbal command movements) and during finger bending/unbending movements. Their results showed that the depth of the posterior part of the left intraparietal sulcus and the bilateral precunei were activated during both imitation and verbal command movements and they have concluded that both these regions were the neural substrates for IP. These findings make sense since the principal functions of the intraparietal sulcus are related to perceptual-

motor coordination (for directing eye movements and reaching) and visual attention (Culham et al., 2001). This being said, the methodology used in Makuuchi’s study is not ideal if one wants to determine the neural substrates of IP: the stimuli used for both verbal commands were names of things represented by the hand postures or directions of the finger/wrist configurations (e.g. stone, scissors, paper, OK, four fingers…), the pictures of the hand postures were the same as the verbal commands; this means that there was no task of tool-use in this study. This is problematic because by definition, IMA is a disorder characterized by the inability to pantomime, imitate, and use tools properly. If one wants to uncover the neural substrates of ideomotor praxis, then one needs to use a complete set of stimuli that will validate every part of the IMA (or praxis) definition including the inability to use tools on demand. There is a variety of other brain areas where lesions have been correlated to IMA such as damage to the angular gyrus, to the supramarginal gyrus, to lateral anterior frontal areas, and sometimes to the supplementary motor area. Lesions to the trunk and splenium of the corpus callosum can also induce apraxic-like behaviors; however, this finding was based on a case study which limits its generalizability (Wheaton et al., 2007). Although numerous studies have looked at the contribution of cortical lesions to IMA, few have systematically studied apraxia following subcortical lesions and most of them have reported isolated individual cases (Wheaton et al., 2007). A review of 82 cases of deep-apraxia showed that IMA was most commonly associated with cortical lesions, which extended to the lenticular nucleus or to the putamen. In these cases however, there was often additional involvement of capsular, periventricular or peristriatal white matter (Pramstaller and Marsden, 1996). Lesions of the thalamus were also found to cause apraxia even if there was no apparent involvement of white matter. The pulvinar nucleus of the thalamus and its connections with both the inferior parietal cortex and the lateral prefrontal cortex (cortical regions traditionally involved in praxis) has been implicated in cases of thalamic apraxia

(Nadeau et al., 1994; Shuren et al., 1994). In regard to subcortical white matter, the corticocortical fibre pathways (which are important for motor control) pass through the peristriatal white matter, and it has been proposed that damage to these fibre bundles by deep lesions may account for the associated IMA (Della Sala et al., 1992). Lesions to the basal ganglia may also play a role in causing IMA, although there is considerable debate as to whether damage to the basal ganglia alone would be sufficient to induce apraxia (Hanna-Pladdy et al., 2005), besides, lesions confined to the basal ganglia that were associated with apraxia are rare. Despite these findings, lesions to these lower brain structures has not, however, been shown to be prevalent in apraxic patients (Hanna-Pladdy et al., 2005; Wheaton et al., 2007). Nonetheless, a study by Hanna-Pladdy et al., (2001) revealed a significant role of subcortical lesions in inducing apraxia. The goal of their study was to ascertain the role of subcortical structures in praxis, and to do so, they compared praxis performance on a variety of tasks in patients with left hemisphere cortical or subcortical lesions (lesion to the basal ganglia). The results showed that the cortical patients presented with deficits in the production of transitive and intransitive gestures to verbal command and imitation, as well as impaired gesture discrimination (transitive gestures being actions using a tool and intransitive ones, actions without the use of a tool). In contrast, the subcortical group demonstrated mild production-execution deficits for transitive pantomimes, but normal imitation and discrimination. Analysis of the types of production errors deficits revealed that both patient groups produced timing errors and the full range of spatial errors. Furthermore, whereas the subcortical group made more postural errors than the cortical group, sequencing, no-response errors and unrecognizable errors were only produced by the cortical group. The different profiles of praxis deficits associated with cortical and subcortical lesions, suggest that these structures may play different roles in praxis. They also

suggested that the basal ganglia motor circuit may be involved in the selection of specific individual object-oriented responses of learned skilled movements. One of the strengths of this study was the N used (n cortical damage =10; n subcortical damage= 9) given that in the few studies that have systematically examined apraxia following subcortical lesions, most reports consisted of isolated individual patients (Hanna-Pladdy et al., 2001). Another strength of the study is the use of a variety of tasks since many lesion localization studies of apraxia used onedimensional assessments of the praxis system and have failed to include a range of task demands designed to fractionate various modules of the praxis system (Roy et al., 2000), and since many investigations primarily used the imitation of intransitive gestures but not other gestures (Hanna-Pladdy et al., 2001). Furthermore, these investigations analyzed apraxia quantitatively and utilized rigid cut-off scores, rather than conceptualizing apraxia as on a continuum of gestural performances; Hanna-Pladdy et al. (2005) opted for a qualitative analysis of error types which allowed them to establish subtypes of IMA. This being said, this study has a weakness: the cortical lesion group was selected based on their stroke lesion size in the left hemisphere but no precise cortical location was mentioned in the article. Also, participants that had subcortical lesions were selected only if they had small ischaemic infarctions primarily in the left striatocapsular area; therefore, persons who had thalamic, periventricular white matter and insular injuries were excluded from this study. Although this narrow selection of participants is justifiable in terms of the maximization of experimental control and perhaps in terms of financial limits, the role of important other subcortical structures (e.g. the thalamus) was not explored but seems nevertheless to be important in understanding IMA. Concluding thoughts Despite the pertinence of lesion studies, it is indeed difficult to study isolated cortical lesions as they often co-occur with subcortical ones and a same lesion can cause different behavioral outputs from

one person to another (Wheaton et al.2007), which somewhat limits the informativeness of these studies. In my opinion, it appears logical and intuitive that subcortical areas are implicated in praxis. For example, praxis requires paying attention to a target stimulus (e.g., a comb) and attention in motor responses has been linked to frontoparietal activation by neuroimaging studies (Jueptner et al., 1997; Rowe et al., 2002); however attention is tightly linked to motivation, which is (among other things) mediated by the nucleus accumbens (a subcortical area). It is also fair to suspect a role of the hippocampus in praxis (and IMA) due to its role in the storing and processing of spatial information. Finally, the cerebellum is also probably involved in praxis and IMA due to its role in procedural learning (personnal communication: Dr. Jim Pfaus). Moreover, I believe that it is not conceptually ideal to isolate the cortical from the subcortical contributions to praxis. It would be more pertinent to study the whole system as an entity on its own since ecologically speaking, brain areas never work in isolation from one another; and because of these inter-areas interactions, synergistic effects can take place where the whole is different from the sum of its parts, and by studying only the parts, we might miss out on the “real” story. Perhaps conducting diffusion-tensor MRI studies would be interesting as it would help to uncover the activity of cooperative regions involved in praxis and their connections. Finally, IMA often co-occurs with neurodegenerative disorders such as Parkinson’s disease, Alzheimer’s disease, corticobasal degeneration, progressive supranuclear palsy and Huntington’s disease (Wheaton et al., 2007). This hints that when considering the biological etiology of IMA, future studies should not restrictively focus on lesions to specific regions of the brain but should also focus on metabolic changes in the brain e.g., Parkinson’s disease is characterized by a dopamine misbalance, which in turns could contribute to IMA since dopamine is implicated in motor control (personal communication, NRL course)…

References

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