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 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.

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.

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.

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.

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.

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.

To Watch is to Work: a Review of NeuroImaging Data on Tool Use Observation Network.

Since the discovery of mirror neurons in the 1990s, many neuroimaging studies have tackled the issue of action observation with the aim of unravelling a putative homolog human system. However, these studies do not distinguish between non-tool-use versus tool-use actions, implying that a common brain network is systematically involved in the observation of any action. Here we provide evidence for a brain network dedicated to tool-use action observation, called the tool-use observation network, mostly situated in the left hemisphere, and distinct from the non-tool-use action observation network. Areas specific for tool-use action observation are the left cytoarchitectonic area PF within the left inferior parietal lobe and the left inferior frontal gyrus. The neural correlates associated with the observation of tool-use reported here offer new insights into the neurocognitive bases of action observation and tool use, as well as addressing more fundamental issues on the origins of specifically human phenomena such as cumulative technological evolution.

Novel Tool Selection in Left Brain-Damaged Patients With Apraxia of Tool Use: A Study of Three Cases.

OBJECTIVES: Recent evidence indicates that some left brain-damaged (LBD) patients have difficulties to use familiar tools because of the inability to reason about physical object properties. A fundamental issue is to understand the residual capacity of those LBD patients in tool selection. METHODS: Three LBD patients with tool use disorders, three right brain-damaged (RBD) patients, and six matched healthy controls performed a novel tool selection task, consisting in extracting a target out from a box by selecting the relevant tool among eight, four, or two tools. Three criteria were manipulated to make relevant and irrelevant tools (size, rigidity, shape). RESULTS: LBD patients selected a greater number of irrelevant tools and had more difficulties to solve the task compared to RBD patients and controls. All participants committed more errors for selecting relevant tools based on rigidity and shape than size. In some LBD patients, the difficulties persisted even in the 2-Choice condition. CONCLUSIONS: Our findings confirm that tool use disorders result from impaired technical reasoning, leading patients to meet difficulties in selecting tools based on their physical properties. We also go further by showing that these difficulties can decrease as the choice is reduced, at least for some properties, opening new avenues for rehabilitation programs. (JINS, 2018, 24, 524-529).

Current standards of neuropsychological assessment in epilepsy surgery centers across Europe.

We explored the current practice with respect to the neuropsychological assessment of surgical epilepsy patients in European epilepsy centers, with the aim of harmonizing and establishing common standards. Twenty-six epilepsy centers and members of "E-PILEPSY" (a European pilot network of reference centers in refractory epilepsy and epilepsy surgery), were asked to report the status of neuropsychological assessment in adults and children via two different surveys. There was a consensus among these centers regarding the role of neuropsychology in the presurgical workup. Strong agreement was found on indications (localization, epileptic dysfunctions, adverse drugs effects, and postoperative monitoring) and the domains to be evaluated (memory, attention, executive functions, language, visuospatial skills, intelligence, depression, anxiety, and quality of life). Although 186 different tests are in use throughout these European centers, a core group of tests reflecting a moderate level of agreement could be discerned. Variability exists with regard to indications, protocols, and paradigms for the assessment of hemispheric language dominance. For the tests in use, little published evidence of clinical validity in epilepsy was provided. Participants in the survey reported a need for improvement concerning the validity of the tests, tools for the assessment of everyday functioning and accelerated forgetting, national norms, and test co-normalization. Based on the present survey, we documented a consensus regarding the indications and principles of neuropsychological testing. Despite the variety of tests in use, the survey indicated that there may be a core set of tests chosen based on experience, as well as on published evidence. By combining these findings with the results of an ongoing systematic literature review, we aim for a battery that can be recommended for the use across epilepsy surgical centers in Europe.

Involvement of the Left Supramarginal Gyrus in Manipulation Judgment Tasks: Contributions to Theories of Tool Use.

OBJECTIVES: Two theories of tool use, namely the gesture engram and the technical reasoning theories, make distinct predictions about the involvement of the left inferior parietal lobe (IPL) in manipulation judgement tasks. The objective here is to test these alternative predictions based on previous studies on manipulation judgment tasks using transcranial magnetic stimulations (TMS) targeting the left supramarginal gyrus (SMG). METHODS: We review recent TMS studies on manipulation judgement tasks and confront these data with predictions made by both tool use theories. RESULTS: The left SMG is a highly intertwined region, organized following several functionally distinct areas and TMS may have disrupted a cortical network involved in the ability to use tools rather than only one functional area supporting manipulation knowledge. Moreover, manipulation judgement tasks may be impaired following virtual lesions outside the IPL. CONCLUSIONS: These data are more in line with the technical reasoning hypothesis, which assumes that the left IPL does not store manipulation knowledge per se. (JINS, 2017, 23, 685-691).

Rethinking the Cognitive Mechanisms Underlying Pantomime of Tool Use: Evidence from Alzheimer's Disease and Semantic Dementia.

OBJECTIVES: Pantomiming the use of familiar tools is a central test in the assessment of apraxia. However, surprisingly, the nature of the underlying cognitive mechanisms remains an unresolved issue. The aim of this study is to shed a new light on this issue by exploring the role of functional, mechanical, and manipulation knowledge in patients with Alzheimer's disease and semantic dementia and apraxia of tool use. METHODS: We performed multiple regression analyses with the global performance and the nature of errors (i.e., production and conception) made during a pantomime of tool use task in patients and control participants as dependent variables and tasks investigating functional, mechanical, and manipulation knowledge as predictors. RESULTS: We found that mechanical problem solving, assessing mechanical knowledge, was a good predictor of the global performance of pantomime of tool use. We also found that occurrence of conception errors was robustly predicted by the task assessing functional knowledge whereas that of production errors was not explained by only one predictor. CONCLUSIONS: Our results suggest that both functional and mechanical knowledge are important to pantomime the use of tools. To our knowledge, this is the first demonstration that mechanical knowledge plays a role in pantomime of tool use. Although impairment in pantomime of tool use tasks (i.e., apraxia) is widely explained by the disruption of manipulation knowledge, we propose that pantomime of tool use is a complex problem-solving task. (JINS, 2017, 23, 128-138).

Imitation and matching of meaningless gestures: distinct involvement from motor and visual imagery.

The aim of the present study was to understand the underlying cognitive processes of imitation and matching of meaningless gestures. Neuropsychological evidence obtained in brain damaged patients, has shown that distinct cognitive processes supported imitation and matching of meaningless gestures. Left-brain damaged (LBD) patients failed to imitate while right-brain damaged (RBD) patients failed to match meaningless gestures. Moreover, other studies with brain damaged patients showed that LBD patients were impaired in motor imagery while RBD patients were impaired in visual imagery. Thus, we hypothesize that imitation of meaningless gestures might rely on motor imagery, whereas matching of meaningless gestures might be based on visual imagery. In a first experiment, using a correlational design, we demonstrated that posture imitation relies on motor imagery but not on visual imagery (Experiment 1a) and that posture matching relies on visual imagery but not on motor imagery (Experiment 1b). In a second experiment, by manipulating directly the body posture of the participants, we demonstrated that such manipulation evokes a difference only in imitation task but not in matching task. In conclusion, the present study provides direct evidence that the way we imitate or we have to compare postures depends on motor imagery or visual imagery, respectively. Our results are discussed in the light of recent findings about underlying mechanisms of meaningful and meaningless 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.

Apraxia and Alzheimer's disease: review and perspectives.

Apraxia is one of the cognitive deficits that characterizes Alzheimer's disease. Despite its prevalence and relevance to diagnosing Alzheimer's disease, this topic has received little attention and is without comprehensive review. The review herein is aimed to fill this gap by first presenting an overview of the impairment caused in different clinical situations: pantomime of tool use, single tool use, real tool use, mechanical problem solving, function and manipulation knowledge tasks, and symbolic/meaningless gestures. On the basis of these results, we then propose alternative interpretations regarding the nature of the underlying mechanisms impaired by the disease. Also presented are principal methodological issues precluding firm conclusions from being drawn.

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.

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.

Visual memory and visual perception: when memory improves visual search.

This study examined the relationship between memory and perception in order to identify the influence of a memory dimension in perceptual processing. Our aim was to determine whether the variation of typical size between items (i.e., the size in real life) affects visual search. In two experiments, the congruency between typical size difference and perceptual size difference was manipulated in a visual search task. We observed that congruency between the typical and perceptual size differences decreased reaction times in the visual search (Exp. 1), and noncongruency between these two differences increased reaction times in the visual search (Exp. 2). We argue that these results highlight that memory and perception share some resources and reveal the intervention of typical size difference on the computation of the perceptual size difference.

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.