Visuo-spatial complexity potentiates the body-part effect in intransitive imitation of meaningless gestures.

Recent studies on the imitation of intransitive gestures suggest that the body part effect relies mainly upon the direct route of the dual-route model through a visuo-transformation mechanism. Here, we test the visuo-constructive hypothesis which posits that the visual complexity may directly potentiate the body part effect for meaningless gestures. We predicted that the difference between imitation of hand and finger gestures would increase with the visuo-spatial complexity of gestures. Second, we aimed to identify some of the visuo-spatial predictors of meaningless finger imitation skills. Thirty-eight participants underwent an imitation task containing three distinct set of gestures, that is, meaningful gestures, meaningless gestures with low visual complexity, and meaningless gestures with higher visual complexity than the first set of meaningless gestures. Our results were in general agreement with the visuo-constructive hypothesis, showing an increase in the difference between hand and finger gestures, but only for meaningless gestures with higher visuo-spatial complexity. Regression analyses confirm that imitation accuracy decreases with resource-demanding visuo-spatial factors. Taken together, our results suggest that the body part effect is highly dependent on the visuo-spatial characteristics of the gestures.

The neural correlates of limb apraxia: An anatomical likelihood estimation meta-analysis of lesion-symptom mapping studies in brain-damaged patients.

Limb apraxia is a motor disorder frequently observed following a stroke. Apraxic deficits are classically assessed with four tasks: tool use, pantomime of tool use, imitation, and gesture understanding. These tasks are supported by several cognitive processes represented in a left-lateralized brain network including inferior frontal gyrus, inferior parietal lobe (IPL), and lateral occipito-temporal cortex (LOTC). For the past twenty years, voxel-wise lesion symptom mapping (VLSM) studies have been used to unravel the neural correlates associated with apraxia, but none of them has proposed a comprehensive view of the topic. In the present work, we proposed to fill this gap by performing a systematic Anatomic Likelihood Estimation meta-analysis of VLSM studies which included tasks traditionally used to assess apraxia. We found that the IPL was crucial for all the tasks. Moreover, lesions within the LOTC were more associated with imitation deficits than tool use or pantomime, confirming its important role in higher visual processing. Our results questioned traditional neurocognitive models on apraxia and may have important clinical implications.

The Neurocognitive Bases of Meaningful Intransitive Gestures: A Systematic Review and Meta-analysis of Neuropsychological Studies.

Researchers and clinicians have long used meaningful intransitive (i.e., not tool-related; MFI) gestures to assess apraxia-a complex and frequent motor-cognitive disorder. Nevertheless, the neurocognitive bases of these gestures remain incompletely understood. Models of apraxia have assumed that meaningful intransitive gestures depend on either long-term memory (i.e., semantic memory and action lexicons) stored in the left hemisphere, or social cognition and the right hemisphere. This meta-analysis of 42 studies reports the performance of 2659 patients with either left or right hemisphere damage in tests of meaningful intransitive gestures, as compared to other gestures (i.e., MFT or meaningful transitive and MLI or meaningless intransitive) and cognitive tests. The key findings are as follows: (1) deficits of meaningful intransitive gestures are more frequent and severe after left than right hemisphere lesions, but they have been reported in both groups; (2) we found a transitivity effect in patients with lesions of the left hemisphere (i.e., meaningful transitive gestures more difficult than meaningful intransitive gestures) but a "reverse" transitivity effect in patients with lesions of the right hemisphere (i.e., meaningful transitive gestures easier than meaningful intransitive gestures); (3) there is a strong association between meaningful intransitive and transitive (but not meaningless) gestures; (4) isolated deficits of meaningful intransitive gestures are more frequent in cases with right than left hemisphere lesions; (5) these deficits may occur in the absence of language and semantic memory impairments; (6) meaningful intransitive gesture performance seems to vary according to the emotional content of gestures (i.e., body-centered gestures and emotional valence-intensity). These findings are partially consistent with the social cognition hypothesis. Methodological recommendations are given for future studies.

Knowing "what for," but not "where": Dissociation between functional and contextual tool knowledge in healthy individuals and patients with dementia.

OBJECTIVE: Semantic tool knowledge underlies the ability to perform activities of daily living. Models of apraxia have emphasized the role of functional knowledge about the action performed with tools (e.g., a hammer and a mallet allow a "hammering" action), and contextual knowledge informing individuals about where to find tools in the social space (e.g., a hammer and a mallet can be found in a workshop). The goal of this study was to test whether contextual or functional knowledge, would be central in the organization of tool knowledge. It was assumed that contextual knowledge would be more salient than functional knowledge for healthy controls and that patients with dementia would show impaired contextual knowledge. METHODS: We created an original, open-ended categorization task with ambiguity, in which the same familiar tools could be matched on either contextual or functional criteria. RESULTS: In our findings, healthy controls prioritized a contextual, over a functional criterion. Patients with dementia had normal visual categorization skills (as demonstrated by an original picture categorization task), yet they made less contextual, but more functional associations than healthy controls. CONCLUSION: The findings support a dissociation between functional knowledge ("what for") on the one hand, and contextual knowledge ("where") on the other hand. While functional knowledge may be distributed across semantic and action-related factors, contextual knowledge may actually be the name of higher-order social norms applied to tool knowledge. These findings may encourage researchers to test both functional and contextual knowledge to diagnose semantic deficits and to use open-ended categorization tests.

Sensory Integration Deficits in Neurodegenerative Diseases: Implications for Apraxia.

OBJECTIVE: Apraxia is the inability to perform voluntary, skilled movements following brain lesions, in the absence of sensory integration deficits. Yet, patients with neurodegenerative diseases (ND) may have sensory integration deficits, so we tested the associations and dissociations between apraxia and sensory integration. METHODS: A total of 44 patients with ND and 20 healthy controls underwent extensive testing of sensory integration (i.e., localization of tactile, visual, and proprioceptive stimuli; agraphesthesia; astereognosis) and apraxia (i.e., finger dexterity, imitation, tool use). RESULTS: The results showed (i) that patients with Alzheimer's disease, corticobasal syndrome, or posterior cortical atrophy were impaired on both dimensions; (ii) An association between both dimensions; (iii) that when sensory integration was controlled for, the frequency of apraxia decreased dramatically in some clinical subgroups. CONCLUSION: In a non-negligible portion of patients, the hypothesis of a disruption of sensory integration can be more parsimonious than the hypothesis of apraxia in case of impaired skilled gestures. Clinicians and researchers are advised to integrate sensory integration measures along with their evaluation of apraxia.

Involvement of the posterior tool processing network during explicit retrieval of action tool and semantic tool knowledge: an fMRI study.

Our ability to understand how to interact with familiar objects is supported by conceptual tool knowledge. Conceptual tool knowledge includes action tool and semantic tool knowledge which are supported by the ventro-dorsal and the ventral pathways, respectively. This apparent functional segregation has been recently called into question. In a block-design fMRI study, 35 participants were asked to complete manipulation, function, and association judgment tasks about pairs of familiar objects. Our results showed that lateral occipitotemporal cortex in the ventral pathway was more sensitive to manipulation and function judgment tasks compared with association judgment tasks. Functional connectivity analyses revealed distinct coupling patterns between inferior parietal lobule, lateral occipitotemporal cortex, and fusiform gyrus. Taken together, these data indicate that action tool and semantic tool knowledge are both supported by ventral and ventro-dorsal pathways. Moreover, the explicit retrieval of these representations is supported by the functional coupling of common and distinct brain regions of the posterior tool processing network varying according to the kind of relations to be retrieved.

Action Observation Network Activity Related to Object-Directed and Socially-Directed Actions in Adolescents.

The human action observation network (AON) encompasses brain areas consistently engaged when we observe other's actions. Although the core nodes of the AON are present from childhood, it is not known to what extent they are sensitive to different action features during development. Because social cognitive abilities continue to mature during adolescence, the AON response to socially-oriented actions, but not to object-related actions, may differ in adolescents and adults. To test this hypothesis, we scanned with functional magnetic resonance imaging (fMRI) male and female typically-developing teenagers (n = 28; 13 females) and adults (n = 25; 14 females) while they passively watched videos of manual actions varying along two dimensions: sociality (i.e., directed toward another person or not) and transitivity (i.e., involving an object or not). We found that action observation recruited the same fronto-parietal and occipito-temporal regions in adults and adolescents. The modulation of voxel-wise activity according to the social or transitive nature of the action was similar in both groups of participants. Multivariate pattern analysis, however, revealed that decoding accuracies in intraparietal sulcus (IPS)/superior parietal lobe (SPL) for both sociality and transitivity were lower for adolescents compared with adults. In addition, in the lateral occipital temporal cortex (LOTC), generalization of decoding across the orthogonal dimension was lower for sociality only in adolescents. These findings indicate that the representation of the content of others' actions, and in particular their social dimension, in the adolescent AON is still not as robust as in adults.SIGNIFICANCE STATEMENT The activity of the action observation network (AON) in the human brain is modulated according to the purpose of the observed action, in particular the extent to which it involves interaction with an object or with another person. How this conceptual representation of actions is implemented during development is largely unknown. Here, using multivoxel pattern analysis (MVPA) of functional magnetic resonance imaging (fMRI) data, we discovered that, while the action observation network is in place in adolescence, the fine-grain organization of its posterior regions is less robust than in adults to decode the abstract social dimensions of an action. This finding highlights the late maturation of social processing in the human brain.

The cortical thickness of the area PF of the left inferior parietal cortex mediates technical-reasoning skills.

Most recent research highlights how a specific form of causal understanding, namely technical reasoning, may support the increasing complexity of tools and techniques developed by humans over generations, i.e., the cumulative technological culture (CTC). Thus, investigating the neurocognitive foundations of technical reasoning is essential to comprehend the emergence of CTC in our lineage. Whereas functional neuroimaging evidence started to highlight the critical role of the area PF of the left inferior parietal cortex (IPC) in technical reasoning, no studies explored the links between the structural characteristics of such a brain region and technical reasoning skills. Therefore, in this study, we assessed participants' technical-reasoning performance by using two ad-hoc psycho-technical tests; then, we extracted from participants' 3 T T1-weighted magnetic-resonance brain images the cortical thickness (i.e., a volume-related measure which is associated with cognitive performance as reflecting the size, density, and arrangement of cells in a brain region) of all the IPC regions for both hemispheres. We found that the cortical thickness of the left area PF predicts participants' technical-reasoning performance. Crucially, we reported no correlations between technical reasoning and the other IPC regions, possibly suggesting the specificity of the left area PF in generating technical knowledge. We discuss these findings from an evolutionary perspective, by speculating about how the evolution of parietal lobes may have supported the emergence of technical reasoning in our lineage.

Meaningless imitation in neurodegenerative diseases: Effects of body part, bimanual imitation, asymmetry, and body midline crossing.

Visuo-imitative apraxia has been consistently reported in patients with dementia, yet there have been substantial methodological differences between studies, while multiple, sometimes competing hypotheses have been put forward to explain this syndrome. Our goals were to study specific imitation deficits in groups of patients who have been selected and assigned to a group solely based on clinical criteria. We tested the effects of body part, bimanual imitation, asymmetry of the model, and body midline crossing, in patients with cortical atrophy of the temporal lobes (semantic dementia, SD), frontal-parietal networks (FPN, i.e., posterior cortical atrophy and corticobasal syndrome) or both (Alzheimer's disease, AD). Sixty-three patients and 32 healthy controls were asked to imitate 45 meaningless finger/hand, uni-/bimanual, asymmetrical/symmetrical, and crossed/uncrossed postures. SD patients had subnormal imitation scores. FPN patients showed frequent and marked deficits in most conditions, better performance with hand than finger postures (probably because of visuo-constructive deficits), and better performance with uncrossed than crossed configurations (probably because of body schema disorganization). Bimanual configurations were difficult for AD patients, not because of bimanual activity in itself, but rather because of the complexity of the model. The finding of dissociations in 34/63 cases (54%) suggests that some patients, even within the same clinical category, can have variable performance in imitation tests as a function of the abovementioned factors. Clinicians are advised to use tests with a large array of items to properly capture patients' imitation skills. This provides a new basis for future research to unpack which neurocognitive mechanisms are disrupted to cause specific patterns of impaired imitation.

On the Neurocognitive Co-Evolution of Tool Behavior and Language: Insights from the Massive Redeployment Framework.

Understanding the link between brain evolution and the evolution of distinctive features of modern human cognition is a fundamental challenge. A still unresolved question concerns the co-evolution of tool behavior (i.e., tool use or tool making) and language. The shared neurocognitive processes hypothesis suggests that the emergence of the combinatorial component of language skills within the frontal lobe/Broca's area made possible the complexification of tool-making skills. The importance of the frontal lobe/Broca's area in tool behavior is somewhat surprising with regard to the literature on neuropsychology and cognitive neuroscience, which has instead stressed the critical role of the left inferior parietal lobe. Therefore, to be complete, any version of the shared neurocognitive processes hypothesis needs to integrate the potential interactions between the frontal lobe/Broca's area and the left inferior parietal lobe as well as their co-evolution at a phylogenetic level. Here, we sought to provide the first elements of answer through the use of the massive deployment framework, which posits that evolutionarily older brain areas are deployed in more cognitive functions (i.e., they are less specific). We focused on the left parietal cortex, and particularly the left areas PF, PGI, and anterior intraparietal (AIP), which are known to be involved in tool use, language, and motor control, respectively. The deployment of each brain area in different cognitive functions was measured by conducting a meta-analysis of neuroimaging studies. Our results confirmed the pattern of specificity for each brain area and also showed that the left area PGI was far less specific than the left areas PF and AIP. From these findings, we discuss the different evolutionary scenarios depicting the potential co-evolution of the combinatorial and generative components of language and tool behavior in our lineage.

Semantic and action tool knowledge in the brain: Identifying common and distinct networks.

Most cognitive models of apraxia assume that impaired tool use results from a deficit occurring at the conceptual level, which contains dedicated information about tool use, namely, semantic and action tool knowledge. Semantic tool knowledge contains information about the prototypical use of familiar tools, such as function (e.g., a hammer and a mallet share the same purpose) and associative relations (e.g., a hammer goes with a nail). Action tool knowledge contains information about how to manipulate tools, such as hand posture and kinematics. The present review aimed to better understand the neural correlates of action and semantic tool knowledge, by focusing on activation, stimulation and patients' studies (left brain-damaged patients). We found that action and semantic tool knowledge rely upon a large brain network including temporal and parietal regions. Yet, while action tool knowledge calls into play the intraparietal sulcus, function relations mostly involve the anterior and posterior temporal lobe. Associative relations engaged the angular and the posterior middle temporal gyrus. Moreover, we found that hand posture and kinematics both tapped into the inferior parietal lobe and the lateral occipital temporal cortex, but no region specificity was found for one or the other representation. Our results point out the major role of both posterior middle temporal gyrus and inferior parietal lobe for action and semantic tool knowledge. They highlight the common and distinct brain networks involved in action and semantic tool networks and spur future directions on this topic.

Physical understanding in neurodegenerative diseases.

This quantitative review gives an overview of physical understanding (i.e., the ability to represent and use the laws of physics to interact with the physical world) impairments in Alzheimer's disease (AD), semantic dementia (SD), and corticobasal syndrome (CBS), as assessed mainly with mechanical problem-solving and tool use tests. This review shows that: (1) SD patients have apraxia of tool use because of semantic tool knowledge deficits, but normal performance in tests of physical understanding; (2) AD and CBS patients show impaired performance in mechanical problem-solving tests, probably not because of intrinsic deficits of physical understanding, but rather because of additional cognitive (AD) or motor impairments (CBS); (3) As a result, the performance in mechanical problem-solving tests is not a good predictor of familiar tool use in dementia; (4) Actual deficits of physical understanding are probably observed only in late stages of neurodegenerative diseases, and associated with functional loss.

Pantomime of tool use: looking beyond apraxia.

Pantomime has a long tradition in clinical neuropsychology of apraxia. It has been much more used by researchers and clinicians to assess tool-use disorders than real tool use. Nevertheless, it remains incompletely understood and has given rise to controversies, such as the involvement of the left inferior parietal lobe or the nature of the underlying cognitive processes. The present article offers a comprehensive framework, with the aim of specifying the neural and cognitive bases of pantomime. To do so, we conducted a series of meta-analyses of brain-lesion, neuroimaging and behavioural studies about pantomime and other related tasks (i.e. real tool use, imitation of meaningless postures and semantic knowledge). The first key finding is that the area PF (Area PF complex) within the left inferior parietal lobe is crucially involved in both pantomime and real tool use as well as in the kinematics component of pantomime. The second key finding is the absence of a well-defined neural substrate for the posture component of pantomime (both grip errors and body-part-as-tool responses). The third key finding is the role played by the intraparietal sulcus in both pantomime and imitation of meaningless postures. The fourth key finding is that the left angular gyrus seems to be critical in the production of motor actions directed towards the body. The fifth key finding is that performance on pantomime is strongly correlated with the severity of semantic deficits. Taken together, these findings invite us to offer a neurocognitive model of pantomime, which provides an integrated alternative to the two hypotheses that dominate the field: The gesture-engram hypothesis and the communicative hypothesis. More specifically, this model assumes that technical reasoning (notably the left area PF), the motor-control system (notably the intraparietal sulcus), body structural description (notably the left angular gyrus), semantic knowledge (notably the polar temporal lobes) and potentially theory of mind (notably the middle prefrontal cortex) work in concert to produce pantomime. The original features of this model open new avenues for understanding the neurocognitive bases of pantomime, emphasizing that pantomime is a communicative task that nevertheless originates in specific tool-use (not motor-related) cognitive processes. .

Daily life activities in patients with Alzheimer's disease or semantic dementia: Multitasking assessment.

The aim of the present study was to compare patients with mild to moderate Alzheimer's disease (AD) or semantic dementia (SD) on their cognitive processes and the severity of their daily life activity impairments. Three types of tasks were administered to patients (SD = 15; AD = 31) and 30 healthy controls (HC): 1) informant-based scales and questionnaires, 2) a neuropsychological assessment exploring executive functions, episodic and semantic memory, and 3) a new original test featuring multi-step naturalistic actions and multitasking: the Sequential Daily Life Multitasking (SDLM). We predicted that patients with AD would mainly exhibit task perplexity, associated with episodic and executive deficits on the SDLM, while the behavior of patients with SD would mostly be characterized by object perplexity, associated with semantic memory deficits. Results showed that patients with AD or SD were impaired across all neuropsychological tests, particularly episodic memory in AD and semantic memory in SD. General performance on the SDLM also appeared dramatically impaired in both patient groups, and correlated with results of questionnaires about instrumental activities and memory impairments. However, specific qualitative measurements on the SDLM did not allow us to pinpoint different patterns of errors and behavior in patients with AD versus SD. We suggest that the inability of patients in both groups to perform the SDLM may derive from a constellation of disorders or else from more subtle impairment of cognitive and conative processes that requires further exploration.

Using tools effectively despite defective hand posture: A single-case study.

Apraxia, a cognitive disorder of motor control, can severely impair transitive actions (object-related) and may lead to action errors (e.g., rubbing a hammer on a nail instead of pounding it) and hand posture errors (e.g., grasping a tool in a wrong way). Here, we report a rare observation of a left-handed patient, left-lateralized for language, who developed a severe apraxia following a right brain lesion. Interestingly the patient showed a significant number of hand posture errors, while she perfectly demonstrated the actual use of tools. This case stressed the predictions made by the current theories of tool use. According to the manipulation-based approach, the hand posture errors should be associated with an impaired manipulation knowledge. According to the reasoning-based approach, the absence of action errors should be associated with spared mechanical knowledge. Moreover, to better understand the neurocognitive origins of the deficit observed in VF, we examined several potential brain lateralization of praxis functions. We initiated a systematic examination of VF's performance in several contexts of tool use allowing us to investigate which kinds of tool-use representations were potentially impaired in VF. Our investigation did not reveal any major deficit of manipulation knowledge. This can hardly account for the high frequency of hand posture errors, contrary to the predictions of the manipulation-based approach. In contrast, in line with the reasoning-based approach, mechanical knowledge was spared and can explain the absence of action errors. We also found that VF probably had a bilateral organization of praxis functions, but irrespective of the possible brain lateralization considered, none of which established a satisfactory association between manipulation knowledge and hand posture errors. Taken together, the manipulation-based approach fails to explain fully the deficit presented by this patient and should lead us to consider alternative explanations.

Technition: When Tools Come Out of the Closet.

People are ambivalently enthusiastic and anxious about how far technology can go. Therefore, understanding the neurocognitive bases of the human technical mind should be a major topic of the cognitive sciences. Surprisingly, however, scientists are not interested in this topic or address it only marginally in other mainstream domains (e.g., motor control, action observation, social cognition). In fact, this lack of interest may hinder our understanding of the necessary neurocognitive skills underlying our appetence for transforming our physical environment. Here, we develop the thesis that our technical mind originates in perhaps uniquely human neurocognitive skills, namely, technical-reasoning skills involving the area PF within the left inferior parietal lobe. This thesis creates an epistemological rupture with the state of the art that justifies the emergence of a new field in the cognitive sciences (i.e., technition) dedicated to the intelligence hidden behind tools and other forms of technologies, including constructions.

Effect of object substitution, spontaneous compensation and repetitive training on reaching movements in a patient with optic ataxia.

We report the case of M.B. who demonstrated severe optic ataxia with the right hand following stroke in the left hemisphere. The clinical picture may shed light on both the pathological characteristics of reaching and grasping actions, and potential rehabilitation strategies for optic ataxia. First, M.B. demonstrated a dissociation between severely impaired reaching and relatively spared grasping and tool use skills and knowledge, which confirms that grasping may be more intermingled with non-motoric cognitive mechanisms than reaching. Besides, M.B.'s reaching performance was sensitive to movement repetition. We observed a substitution effect: Reaching time decreased if M.B. repeatedly reached toward the same object but increased when object identity changed. This may imply that not only object localization but also object identity, is integrated into movement programming in reach-to-grasp tasks. Second, studying M.B.'s spontaneous compensation strategies ascertained that the mere repetition of reaching movements had a positive effect, to the point M.B. almost recovered to normal level after an intensive one-day repetitive training session. This case study seems to provide one of the first examples of optic ataxia rehabilitation. Reaching skills can be trained by repetitive training even two years post-stroke and despite the presence of visuo-imitative apraxia.

Imitation of meaningless gestures in normal aging.

While imitation of meaningless gestures is a gold standard in the assessment of apraxia in patients with either stroke or neurodegenerative diseases, little is known about potential age-related effects on this measure. A significant body of literature has indicated that different mechanisms (i.e., executive functioning, visuospatial skills, sensory integration, body knowledge, categorical apprehension) may underlie the performance depending on imitation conditions (i.e., finger/hand, uni-/bimanual, symmetric/asymmetric, crossed/uncrossed configurations). However, neither the effects of these conditions on performance, nor the contribution of the abovementioned mechanisms to imitation have been explored in normal aging. The aim of the present study was to fill this gap. To do so, healthy adults (n = 103) aged 50 to 89 were asked to imitate 45 meaningless gestures. The authors controlled for general cognitive function, motor function, visual-spatial skills, executive function, sensory integration, body knowledge, and mechanical problem-solving skills. The results showed that asymmetry, body-midline crossing and, to a lesser extent, bimanual activity added an additional layer of difficulty to imitation tasks. After controlling for motor speed and cognitive function, age had an effect on imitation skills after 70 years old. This may reflect a decline in body knowledge, sensory integration, and executive functions. In contrast, the visuospatial and mechanical problem-solving hypotheses were ruled out. An additional motor simulation hypothesis is proposed. These findings may prove useful for clinicians working in memory clinics by providing insights on how to interpret imitation deficits. Lower performance after 70 years old should not be considered abnormal in a systematic manner.