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The – weak – role of memory in tool use: Evidence from neurodegenerative diseases

Published on Jun 1, 2019in Neuropsychologia2.872
· DOI :10.1016/j.neuropsychologia.2019.03.008
Josselin Baumard6
Estimated H-index: 6
,
Mathieu Lesourd11
Estimated H-index: 11
(University of Lyon)
+ 8 AuthorsDidier Le Gall20
Estimated H-index: 20
(University of Angers)
Abstract
Abstract Objective Although tool use disorders are frequent in neurodegenerative diseases, the question of which cognitive mechanisms are at stake is still under debate. Memory-based hypotheses (i.e., the semantic knowledge hypothesis and the manipulation knowledge hypothesis) posit that tool use relies solely on stored information about either tools or gestures whereas a reasoning-based hypothesis (i.e., the technical-semantic hypothesis) suggests that loss of semantic knowledge can be partially compensated by technical reasoning about the physical properties of tools and objects. Method These three hypotheses were tested by comparing performance of 30 healthy controls, 30 patients with Alzheimer's disease and 13 patients with semantic dementia in gesture production tasks (i.e., pantomime of tool use, single tool use, real tool use) and tool or gesture recognition tasks (i.e., functional and contextual matching, recognition of tool manipulation). Individual, item-based patterns of performance were analyzed to answer the following question: Could participants demonstrate the use of tools about which they had lost knowledge? With this aim in mind, “validation” and “rebuttal” frequencies were calculated based on each prediction. Results Predictions from the technical-semantic hypothesis were more frequently observed than memory-based predictions. A number of patients were able to use and demonstrate the use of tools for which they had lost either semantic or manipulation knowledge (or both). Conclusions These data lead to question the role of different types of memory in tool use. The hypothesis of stored, tool-specific knowledge does not predict accurately clinical performances at the individual level. This may lead to explore the influence of either additional memory systems (e.g., personal/impersonal memory) or other modes of reasoning (e.g., theory of mind) on tool use skills.
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References90
Newest
#1Josselin BaumardH-Index: 6
#2Mathieu Lesourd (University of Lyon)H-Index: 11
Last. Didier Le Gall (University of Angers)H-Index: 20
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Recent works showed that tool use can be impaired in stroke patients because of either planning or technical reasoning deficits, but these two hypotheses have not yet been compared in the field of neurodegenerative diseases. The aim of this study was to address the relationships between real tool use, mechanical problem-solving, and planning skills in patients with Alzheimer's disease (AD, n = 32), semantic dementia (SD, n = 16), and corticobasal syndrome (CBS, n = 9). Patients were asked to sel...
6 CitationsSource
#1Hannah E. Thompson (University of Surrey)H-Index: 6
#2Azizah Almaghyuli (Ebor: University of York)H-Index: 2
Last. Elizabeth Jefferies (Ebor: University of York)H-Index: 38
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Semantic cognition, as described by the controlled semantic cognition (CSC) framework (Rogers et al., 2015, Neuropsychologia, 76, 220), involves two key components: activation of coherent, generalizable concepts within a heteromodal ‘hub’ in combination with modality-specific features (spokes), and a constraining mechanism that manipulates and gates this knowledge to generate time- and task-appropriate behaviour. Executive–semantic goal representations, largely supported by executive regions suc...
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#1François Osiurak (Institut Universitaire de France)H-Index: 3
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#1Lang Chen (Stanford University)H-Index: 9
#2Matthew A. Lambon Ralph (University of Manchester)H-Index: 72
Last. Timothy T. Rogers (UW: University of Wisconsin-Madison)H-Index: 34
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Chen et al. construct a model of the neural bases of semantic representation that unifies domain-specific (distinct systems represent different kinds of things) and domain-general (knowledge for all kinds is encoded in a single network) accounts.
34 CitationsSource
#1R. Shayna RosenbaumH-Index: 30
#2Alice S. N. KimH-Index: 6
Last. Stevenson BakerH-Index: 1
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Much of the richness in human life derives from episodic memory , mental representations of detailed experiences from our personal pasts. To make sense of those experiences, knowledge about the world and oneself must also exist in a form that is free of context – known as semantic memory . This chapter revisits and builds on Tulving's distinction between episodic and semantic memory, with a focus on their differences, similarities, and interactions, informed by cognitive, neuropsychological, and...
Source
Our ability to use conceptual knowledge to support various behaviours is termed semantic cognition. In this Review, Lambon Ralph et al. argue that this ability arises from two interacting neural systems, one for representation and one for control.
289 CitationsSource
#1Josselin Baumard (University of Angers)H-Index: 6
#2Mathieu Lesourd (University of Lyon)H-Index: 11
Last. Didier Le Gall (University of Angers)H-Index: 20
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In the field of apraxia, it has been suggested that the ability to use tools and objects in daily life depends not only on semantic knowledge about tool function and context of use but also on technical reasoning about mechanical properties of tools and objects. The aim of the present work was to assess tool use abilities regarding these hypotheses in patients with neurodegenerative diseases and reduced autonomy. Performance of patients with Alzheimer’s disease (n = 31), semantic dementia (n = 1...
13 CitationsSource
#1Emanuelle Reynaud (University of Lyon)H-Index: 7
#2Mathieu Lesourd (University of Lyon)H-Index: 11
Last. François Osiurak (Institut Universitaire de France)H-Index: 15
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Since more than a century, neuropsychological models have assumed that the left inferior parietal cortex is central to tool use by storing manipulation knowledge (the manipulation-based approach). Interestingly, recent neuropsychological evidence indicates that the left inferior parietal cortex might rather support the ability to reason about physical object properties (the reasoning-based approach). Historically, these two approaches have been developed from data obtained in left brain-damaged ...
45 CitationsSource
#1Christophe Jarry (University of Angers)H-Index: 10
#2François Osiurak (University of Lyon)H-Index: 15
Last. Didier Le Gall (University of Angers)H-Index: 20
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Tool use disorders are usually associated with difficulties in retrieving function and manipulation knowledge. Here, we investigate tool use (Real Tool Use, RTU), function (Functional Association, FA) and manipulation knowledge (Gesture Recognition, GR) in 17 left-brain-damaged (LBD) patients and 14 AD patients (Alzheimer disease). LBD group exhibited predicted deficit on RTU but not on FA and GR while AD patients showed deficits on GR and FA with preserved tool use skills. These findings questi...
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Abstract Purpose To investigate the literature for frequencies, profiles and neural correlates of limb and face apraxias in frontotemporal dementia (FTD). Method The search conducted in Ovid Medline, PsycINFO and Scopus yielded 487 non-duplicate records, 43 of which were included in the final analysis. Results Apraxias are evident in diverse forms in all clinical variants of FTD within the first four years of the disease. Face apraxia and productive limb apraxia co-occur in the behavioural and n...
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