Limb apraxia and the left parietal lobe

doi:10.1016/B978-0-444-63622-5.00017-6

Handbook of Clinical Neurology

Volume 151, 2018, Pages 349-363

https://doi.org/10.1016/B978-0-444-63622-5.00017-6 Get rights and content

Abstract

Limb apraxia is a heterogeneous disorder of skilled action and tool use that has long perplexed clinicians and researchers. It occurs after damage to various loci in a densely interconnected network of regions in the left temporal, parietal, and frontal lobes. Historically, a highly classificatory approach to the study of apraxia documented numerous patterns of performance related to two major apraxia subtypes: ideational and ideomotor apraxia. More recently, there have been advances in our understanding of the functional neuroanatomy and connectivity of the left-hemisphere “tool use network,” and the patterns of performance that emerge from lesions to different loci within this network. This chapter focuses on the left inferior parietal lobe, and its role in tool and body representation, action prediction, and action selection, and how these functions relate to the deficits seen in patients with apraxia subsequent to parietal lesions. Finally, suggestions are offered for several future directions that will benefit the study of apraxia, including increased attention to research on rehabilitation of this disabling disorder.

Introduction

Limb apraxia is a heterogeneous disorder historically defined by exclusion: deficits in skilled movement not caused by weakness, deafferentation, abnormal tone or posture, tremors or chorea, intellectual deterioration, or poor comprehension. As a result, it has been difficult for clinicians and researchers to define exactly what apraxia is. Focusing primarily on limb apraxia after left parietal stroke, this chapter examines the neuroanatomic substrates of apraxia, and reviews historical accounts and recent research on the role of the parietal lobe in skilled action. Recent promising approaches to apraxia treatment are briefly considered. In conclusion,it is suggested that much past confusion can be reduced if limb apraxia is considered to consist of two major clusters of behaviors reflecting damage to representational and spatiotemporal components of skilled action, which may be attributed to damage to distinct loci in a distributed left-hemisphere network.

Section snippets

Clinical assessment

In the past century, many types of apraxic deficits have been described (e.g., dressing apraxia, constructional apraxia, oral apraxia). Here we concentrate on apraxia of the limbs as observed in unilateral stroke populations.

Classic theories of apraxia

At the end of the 19th century, the German linguist Heymann Steinthal (1871, p. 458, part 610) described an aphasic musician who had difficulties grasping tools adequately for their use, including his violin. Steinthal proposed that it is not the movement that is inhibited, but the relation of the mechanism with respect to its function, or the relation of the movement towards the object. Steinthal was the first documented scientist to call the dysfunction apraxia (Steinthal, 1871, p. 458, part

Recent research findings relevant to praxis functions of the parietal lobe

Recent data and theoretical models have addressed additional details of the planning and control of skilled action as implemented by the left IPL. In particular, recent evidence has elucidated three important components of skilled actions: (1) representation of tools and the hand as relevant to object manipulation, pantomime, recognition, and imitation; (2) prediction and simulation of movements of the self and others; and (3) selection of actions appropriate to goals and context. The next

Tool and body representations for production, recognition, and learning of actions

Skillful use of tools, pantomime of tool use actions, knowledge and recognition of object-related actions, and imitation of other's actions are three related functions that, as described earlier, are frequently disrupted after left parietal damage. These abilities all rely on memories of tool use actions that are implemented by the left IPL and its connections with the left posterior temporal lobe and left IFG. The characteristics and format (e.g., visuospatial or sensorimotor) of these

Spatiotemporal planning and prediction

The left IPL is also an important locus of processes involved in action planning and prediction. On a number of accounts, predictive sensorimotor control allows the anticipated consequences of movement to serve as a signal to the motor system to correct anticipated errors even before they are produced (Wolpert and Ghahramani, 2000; Kilner et al., 2007). Predictive coding in the parietal lobe has been studied in a number of ways, including anticipation of the grip force needed to lift objects

Action selection

An additional function of the IPL relevant to praxis processing is selection of actions appropriate to task goals and context. Long noted in the literature is the tendency of apraxics with posterior parietal damage to produce multiple responses and to have difficulty selecting appropriate movements (DeRenzi and Lucchelli, 1988). More recently, Rushworth and colleagues (2003) noted that the left IPL is involved in the selection and redirection of movements. A related theoretical and

Rehabilitation strategies

Limb apraxia may affect various aspects of rehabilitation: impaired imitation of movements aggravates physical therapy, difficulties with gesturing complicates communication, and inadequate object use influences independence in activities of daily living. Despite the obvious relevance, advances in evidence-based rehabilitation strategies for patients with limb apraxia are scanty (for reviews, see Buxbaum et al., 2008; Cantagallo et al., 2012). Gesture training (Cubelli et al., 1991; Daumüller

Future directions and conclusions

Historical accounts of apraxia emphasized characterization of apraxia subtypes (e.g., ideational versus ideomotor) on the basis of error types and patterns of performance with pantomime, single objects, and multiple objects. Unfortunately, such accounts have resulted in ongoing confusion in both clinical and research communities. Owing in part to growing sophistication in lesion analysis approaches, which enable greater statistical certainty about brain–behavior relationships, as well as

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When planning functional grasps of tools, right-handed individuals (dextrals) show mostly left-lateralized neural activity in the praxis representation network (PRN), regardless of the used hand. Here we studied whether or not similar cerebral asymmetries are evident in non-righthanded individuals (adextrals). Sixty two participants, 28 righthanders and 34 non-righthanders (21 lefthanders, 13 mixedhanders), planned functional grasps of tools vs. grasps of control objects, and subsequently performed their pantomimed executions, in an event-related functional magnetic resonance imaging (fMRI) project. Both hands were tested, separately in two different sessions, counterbalanced across participants. After accounting for non-functional components of the prospective grasp, planning functional grasps of tools was associated with greater engagement of the same, left-hemisphere occipito-temporal, parietal and frontal areas of PRN, regardless of hand and handedness. Only when the analyses involved signal changes referenced to resting baseline intervals, differences between adextrals and dextrals emerged. Whereas in the left hemisphere the neural activity was equivalent in both groups (except for the occipito-temporo-parietal junction), its increases in the right occipito-temporal cortex, medial intraparietal sulcus (area MIP), the supramarginal gyrus (area PFt/PF), and middle frontal gyrus (area p9-46v) were significantly greater in adextrals. The inverse contrast was empty. Notably, when individuals with atypical and typical hemispheric phenotypes were directly compared, planning functional (vs. control) grasps invoked, instead, significant clusters located nearly exclusively in the left hemisphere of the typical phenotype. Previous studies interpret similar right-sided vs. left-sided increases in neural activity for skilled actions as handedness dependent, i.e., located in the hemisphere dominant for manual skills. Yet, none of the effects observed here can be purely handedness dependent because there were mixed-handed individuals among adextrals, and numerous mixed-handed and left-handed individuals possess the typical phenotype. Thus, our results clearly show that hand dominance has limited power in driving the cerebral organization of motor cognitive functions.
An active inference model of hierarchical action understanding, learning and imitation
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We advance a novel active inference model of the cognitive processing that underlies the acquisition of a hierarchical action repertoire and its use for observation, understanding and imitation. We illustrate the model in four simulations of a tennis learner who observes a teacher performing tennis shots, forms hierarchical representations of the observed actions, and imitates them. Our simulations show that the agent's oculomotor activity implements an active information sampling strategy that permits inferring the kinematic aspects of the observed movement, which lie at the lowest level of the action hierarchy. In turn, this low-level kinematic inference supports higher-level inferences about deeper aspects of the observed actions: proximal goals and intentions. Finally, the inferred action representations can steer imitative responses, but interfere with the execution of different actions. Our simulations show that hierarchical active inference provides a unified account of action observation, understanding, learning and imitation and helps explain the neurobiological underpinnings of visuomotor cognition, including the multiple routes for action understanding in the dorsal and ventral streams and mirror mechanisms.
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La concepción clásica de la semiología neurológica ha relacionado cada región cerebral con una función determinada, permitiendo un diagnóstico topográfico basado en la anamnesis y la exploración. Las más recientes técnicas de neuroimagen funcional han demostrado mecanismos algo más complejos, otorgando un papel predominante a las redes neuronales establecidas entre diversas regiones cerebrales como las principales generadoras de las diferentes funciones. A pesar de ello, el conocimiento de los síndromes topográficos del cerebro, cerebelo y troncoencéfalo sigue siendo fundamental en la aproximación inicial al diagnóstico topográfico y etiológico de los pacientes con síntomas neurológicos. Así, la afectación de la primera motoneurona debe hacer sospechar una lesión en el lóbulo frontal contralateral, la afectación sensitiva debe orientar a una afectación parietal contralateral, la afasia motora a una lesión en el lóbulo frontal dominante, la sensitiva a una en el temporal dominante o los síndromes cruzados a una afectación troncoencefálica.
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Chapter 17 - Limb apraxia and the left parietal lobe

Abstract

Introduction

Section snippets

Clinical assessment

Classic theories of apraxia

Recent research findings relevant to praxis functions of the parietal lobe

Tool and body representations for production, recognition, and learning of actions

Spatiotemporal planning and prediction

Action selection

Rehabilitation strategies

Future directions and conclusions

Brain Cogn

Cortex

Brain Lang

Cogn Brain Res

Cognition

Neuropsychologia

Neuropsychologia

Brain Res

Cortex

Brain Cogn

Brain Res

Neuropsychologia

Curr Opin Neurobiol

Cortex

Neuropsychologia

Neuropsychologia

Cortex

Trends Neurosci

Cortex

Cognition

Neuropsychologia

Trends Cogn Sci

Neuropsychologia

Neuropsychologia

Neuropsychologia

Neuroimage

Trends Neurosci

Cortex

Neuropsychologia

Neuropsychologia

Action anticipation beyond the action observation network: a functional magnetic resonance imaging study in expert basketball players

Eur J Neurosci

Abnormal reliance on object structure in apraxics' learning of novel actions

J Int Neuropsychol Soc

The white matter structural network underlying human tool use and tool understanding

J Neurosci

The use of ecological sounds in facilitation of tool use in apraxia

Apraxien

Der Nervenarzt

Improving ideomotor limb apraxia by electrical stimulation of the left posterior parietal cortex

Brain

Pathways for motion analysis: cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque

J Comp Neurol

Closely overlapping responses to tools and hands in left lateral occipitotemporal cortex

J Neurophysiol

The neural correlates of planning and executing actual tool use

J Neurosci

Aphasia, apraxia, and agnosia: clinical and theoretical aspects

Gesturing and naming: the use of functional knowledge in object identification

Psychol Sci

Ideational apraxia and naturalistic action

Cogn Neuropsychol

Ideomotor apraxia: a call to action

Neurocase

Action knowledge, visuomotor activation, and embodiment in the two action systems

Ann N Y Acad Sci

Treatment of limb apraxia: moving forward to improved action

Am J Phys Med Rehabil

Separable components of object-related gesture production in the left hemisphere

Critical brain regions for tool-related and imitative actions: a componential analysis

Brain

Infants generate goal-based action predictions

Dev Sci

The cognitive rehabilitation of limb apraxia in patients with stroke

Neuropsychol Rehabil

The representation of objects in apraxia: from action execution to error awareness

Frontiers in Human Neuroscience