Apraxia – Agreements and controversies

Apraxia – Agreements and controversies

Accepted Manuscript Discussion Forum - Apraxia - agreements and controversies Georg Goldenberg PII: S0010-9452(14)00175-0 DOI: 10.1016/j.cortex.201...

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Accepted Manuscript Discussion Forum - Apraxia - agreements and controversies Georg Goldenberg PII:

S0010-9452(14)00175-0

DOI:

10.1016/j.cortex.2014.05.010

Reference:

CORTEX 1210

To appear in:

Cortex

Received Date: 10 May 2014 Accepted Date: 13 May 2014

Please cite this article as: Goldenberg G, Discussion Forum - Apraxia - agreements and controversies, CORTEX (2014), doi: 10.1016/j.cortex.2014.05.010. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Discussion Forum - Apraxia - agreements and controversies. Georg Goldenberg Department of Neuropsychology, Bogenhausen Hospital, Munich1

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Department of Neurology, Technical University Munich

The number and diversity of contributions to the Discussion Forum on Apraxia testifies that apraxia still engenders lively discussions and novel explanations after more than 100 years of

important messages and points of controversy.

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1. Imitation

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research and theorizing. In this discussion I will briefly sum up what appeared to me

The contributions focusing on imitation discuss differences between imitation of meaningful and meaningless gestures and the role of body part coding for imitation of meaningless gestures.

Heilman exploits the associationist principle of engrams (or, as he prefers to name them, visuo-kinetic representations) and their connections to describe an alternative account of

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selective impairment or preservation of imitation. He maintains that production of gestures necessitates access to visuo-kinetic movement representations. Imitation may be better preserved than production on command because the demonstration of the gestures provides visual cues that facilitate access, whereas imitation may appear to be selectively impaired

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when impaired visual movement analysis prevents visual access to the movement representation. Defective imitation of meaningless and novel gestures is not considered as a

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manifestation of apraxia.

Tessari and Cubelli's contribution starts from their demonstration that meaningful gestures are treated as if they were meaningless when they are presented intermingled with meaningless gestures. They characterize the choice between the two routes of imitation as "strategic" but insist that, contrary to what I understood from their original publication, "the notion of strategic control refers to the functional organization of the system and not to the

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Georg Goldenberg. Klinik für Neuropsychologie, Klinikum Bogenhausen. Englschalkingerstrasse 77, D 81925

München, Germany. FAX: +4989 9270 2189; E – Mail: [email protected]

ACCEPTED MANUSCRIPT conscious choice of the participants". Their argument aligns the choice between two routes to imitation with a stimulus dependent automatic decision. Rumiati acknowledges the evidence for defective body representations in apraxia but doubts whether they are necessary for apraxia of imitation or whether they can simply co-occur. Moreover she asks whether the body representation deficit concerns the structural description

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of permanent spatial relationships between body parts or the dynamic body image of current position and movements of the arm.

Whereas Rumiati questions the importance of body part coding for imitation, two other contributions speculate that the role of body part coding may extend beyond imitation:

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Osiurak notes that segmentation and combination of body parts is akin to segmentation and combination of functional parts in mechanical reasoning. However, he also points out an important difference between imitation and tool use: In imitation the human body is processed

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as an end and not as a mean as it might be in tool use. Ietswaart and Evans wonder whether defective body part coding would be sufficient for explaining not only defective imitation but also defective pantomime and tool use in "bodily manipulation terms" as "body movement implementation appears central to apraxia".

2. Use of tools and objects

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The thesis that mechanical problem solving is more important than manipulation knowledge for everyday tool use has raised much critique.

Buxbaum defends the importance of modality specific motor information not only for manipulation of tools but also for recognition of objects and for miming their use. She

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recognizes that mechanical problem solving may contribute to some action tasks but explains flexible adaptation of tool use to changing constraints by typicality effects that emerge from

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overlap of prototypical features across the diversity of repeated practice. Schenk endorses the view that the capacity to generate novel actions is crucial for the recognition of tool use as a cognitive capacity, but doubts whether such generative power is really beyond the possibilities of a storehouse of motor skills. He thinks that "distributed representations implemented in a parallel connectionist network" will have the capacity to generate novel outputs for novel inputs and "do the job that Goldenberg reserved for his mechanical problem solving module". Osiurak classifies my proposal that mechanical problem solving applies not only to interactions between external tools and objects but also to the biomechanical relations between body parts as a "strong version" of mechanical reasoning. He derives doubts on the universal role of mechanical problem solving from experiments on grip selection (Rosenbaum

ACCEPTED MANUSCRIPT et al., 1990; Hermsdörfer et al., 1999) and proposes an alternative "weak version". It restricts the role of mechanical problem solving to the generation of a visual representation of the correct motion of the tool but delegates the motor implementation to a "production system" that selects appropriate manual actions independently from mechanical reasoning. Ietswaart and Evans remark that mechanical problem solving can explain actual tool – use

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by inference of function from structure but cannot be applied to performance during pantomime of tool – use where such indicators are not present. Indeed I have argued that the generation of pantomime follows different paths from the generation of real action (see next section).

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Rumiati addresses limits of mechanical problem solving and functional knowledge by asking whether they can explain not only errors with single tool and objects but also errors in naturalistic multi-step actions with multiple objects. She discards the alternative view that

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errors in naturalistic multi-step actions are due to general resource limitations rather than to specific deficits of tool use and posits that the quality of errors is the same for single tool use and multi-step actions.

Like Rumiati et al. (2001) I have observed patients with left brain damage making typical apraxic errors in the context of naturalistic multi-step actions (see, for example, figure 8.1 of

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the book "Apraxia – the cognitive side of motor control"). However, as I discussed in chapter 9 of the book, systematic empirical group studies have yielded disappointingly poor support for the specificity of apraxic errors in naturalistic actions. Other than errors of single tool use they are not restricted to patients with left brain damage and their qualitative analysis revealed

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a uniform prevalence of omissions of action step regardless of localization and aetiology of lesions (Schwartz et al., 1999; Hartmann et al., 2005).

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3. Communicative Gestures – Pantomime of Tool Use The closeness of the relation between motor programs for pantomime and for actual use is a central topic of this section. Buxbaum interprets my formulation "independence of pantomime from motor programs of use" as a complete exclusion of any motor information as sources for the creation of pantomimes." This is a misunderstanding. I did not maintain that motor tool use information is excluded from the generation of pantomime but that its contribution to the generation of pantomime is not mandatory. The controversy about the role of motor information for pantomime relates to hotly debated controversies concerning the structure of semantic memory. While Buxbaum endorses the importance of "engrams", that is, of modality specific traces left by previous sensations or

ACCEPTED MANUSCRIPT motor acts, I give priority to supramodal representations. They may be based on abstract or linguistic units, on combinations of modality specific entries with an amodal hub, or on networks that unify modality specific information. Their decisive property is that they afford processing and storage of information independently from the modality of their acquisition. I posit that the creation of pantomime is mainly based on such supramodal representations.

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Arguably, the postulate of modality specific representation can be classified as "low level" and the alternative explanation by supramodal mechanisms as "high level".

Hermsdörfer considers significant correlations between kinematic parameters of actual and pantomimed execution of tool use as indicators of an underlying basic motor program

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common to both modes. However, they did not probe the kinematic features of non toolrelated motor actions. This leaves open the possibility that the correlations reflect

characteristics of individual movement styles independently of whether they are applied to

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tool use or to any other movements of comparable complexity.

Vingerhoets challenges the seemingly evident links between pantomime and manual skill by fMRI studies in left handed subjects. He has demonstrated that the laterality of activations elicited by pantomimes of tool use corresponds with the laterality of activation induced by word generation but not necessarily with the laterality of handedness. He concludes that the

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concordance between language and pantomime is obligatory. Referring to single clinical observations of left handed patients in whom right brain damage caused apraxia without aphasia, he posits dissociations between the exact locations of their neural substrate within the same hemisphere rather than between their laterality. To my understanding, this explanation is

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not well supported by the anatomical data of such patients, since they show widely distributed large lesions and cover regions that one would expect to cause severe aphasia when occurring in the left hemisphere of a typical right hander (Goldenberg, 2013). However, such cases are

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exceptional and do not alter the main conclusion that pantomime has more in common with language than with superior manual skill of the dominant hand. This conclusion unmistakably favours the cognitive against the motor side of apraxia. Bartolo and Cubelli discuss the greater vulnerability to apraxia of pantomime of tool use than of emblematic ("intransitive") gestures. They agree that pantomime is not identical to replaying the routine motor program of use but must be constructed de novo out of its elements. Maintenance of the elements during construction requires working memory. By contrast emblematic gestures have conventional shapes that are presumably retrieved as connected units and need not be assembled in working memory. This difference can explain the greater vulnerability of pantomime to apraxia. I would like to add that segmentation of the

ACCEPTED MANUSCRIPT compound image of the tool and its use into a limited number of defined elements reduces the load on working memory during construction of the pantomime. Concerning the rare inverse dissociations of defective emblematic gestures but preserved pantomime, Bartolo and Cubelli note that such observations were made in cases of right brain damage or, in one case, autism. They emphasize the role of emblems in social communication

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and speculate that their impairment is part of a general failure of social cognition that is frequent in right brain damage and constitutive for autism. This speculation is reminiscent of Jackson's attribution of propositional expression to the left, and of emotional reactions to the right hemisphere.

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4. Anatomical basis of apraxia

There were few reactions to my proposals concerning different lateralizations of the neural

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substrates of different manifestations of apraxia (Goldenberg, 2014; figure 1). Those who have witnessed the development of cognitive neuroscience since the last decades of the 20th century will appreciate how far it has withdrawn from the traditional preoccupation with hemisphere dominance and laterality. However, Vingerhoets addressed the concordance between the lateralities of apraxia and aphasia (see above), Bartolo and Cubelli speculated that emblematic (intransitive) gestures may depend on right hemisphere (see above), and

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Mutha and Haaland report effects of left but not right parietal lesions (see below). Mutha and Haaland put forward results from experimental studies of movement planning that question the boundary between cognitive and motor aspects. In a series of experiment they have shown that patients with left parietal lesions cannot smoothly adapt repetitive

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grasping to distortions of the target location (Mutha et al., 2011). They reason that the common involvement of parietal cortex in this apparently low level task and in clinical

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apraxia speaks in favour of a continuum between low level motor and high level cognitive aspects of motor planning and refute the alternative proposal that encroachment of the causal lesions of apraxia to motor centres is responsible for the common influence. Sunderland bases a hypothesis about the anatomical fundament of apraxia on the division between ventral and dorsal stream of visual processing. He argues that their functional dichotomy can be applied also to motor control with the ventral stream being responsible for conceptual planning and the dorsal for adaptation of reaching and grasping to structural features of the environment. Apraxia results mainly from lesions in supramarginal and angular gyrus that interrupt the connection between both streams. The suggestion that apraxia can be caused by interruption of the transition from one stream to the other is reminiscent of the

ACCEPTED MANUSCRIPT alleged emergence of "ideo – motor" apraxia from interruption of the posterior to anterior stream of motor control.

5. Cognition, mind, and body Paul Ehling disagrees with my hypothesis that a leading thread of many theories of apraxia is the opposition of a higher cognitive to a lower motor level of action control, and that this

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opposition is grounded in a mind – body dichotomy. He admits that cognitive plans have to be transformed into concrete actions, but denies that the plan itself is directly formulated in terms of muscle movements or that motor programs may play a role in it. In other words, there is no mind – body dichotomy because the explanation considers only one level, which is cognitive.

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However, my hypothesis does not maintain that every theory of apraxia must consider the dichotomy of high and low levels of motor control. I rather suggested that across the manifold

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theories of apraxia there is a tension between high- and low level approaches and that this tension is a driving force of research and theorizing.

References

Goldenberg, G. (2013). Apraxia in left-handers. Brain, 136, 2592-2601.

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Goldenberg, G. Apraxia - the cognitive side of motor control. Cortex, (in press). Hartmann, K., Goldenberg, G., Daumüller, M., & Hermsdörfer, J. (2005). It takes the whole brain to make a cup of coffee: The neuropsychology of naturalistic actions involving technical

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devices. Neuropsychologia, 43, 625-637.

Hermsdörfer, J., Ulrich, S., Marquardt, C., Goldenberg, G., & Mai, N. (1999). Prehension

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with the ipsilesional hand after unilateral brain damage. Cortex, 35, 139-162. Mutha, P. K., Sainburg, R. L., & Haaland, K. Y. (2011). Left parietal regions are critical for adaptive visuomotor control. Journal of Neuroscience, 31, 6972-6981. Rosenbaum, D. A., Marchak, F., Barnes, H. J., Vaughan, J., Slotta, J. D., & Jorgensen, M. J. (1990). Constraints for action selection: Overhand versus underhand grips. In M.Jeannerod (Ed.), Attention and Performance XIII Motor Representation and Control (pp. 321-342). Hilldale: Lawrence Erlbaum. Rumiati, R. I., Zanini, S., Vorano, L., & Shallice, T. (2001). A form of ideatonal apraxia as a selective deficit of contention scheduling. Cognitive Neuropsychology, 18, 617-642.

ACCEPTED MANUSCRIPT Schwartz, M. F., Buxbaum, L. J., Montgomery, M. W., Fitzpatrick-DeSalme, E. J., Hart, T., Ferraro, M. et al. (1999). Naturalistic action production following right hemisphere stroke.

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Neuropsychologia, 37, 51-66.