The case of communicative intransitive gestures: further developments on a dual mechanism for motor control of action in imitation

Imitation is classically thought of as a mechanism that allows learning from demonstration. Several are the models that offer an explanation of how human imitation is accomplished. Observations of brain damaged patients, healthy subjects and brain imaging data can be found in support of both unique mechanistic models and dual route models (Chapter 1) . Two sets of evidence from neuropsychology and normal experimental psychology support the need of independent mechanisms that can account for either imitation of novel, meaningless actions or familiar, meaningful actions..

Brief Report: Visuo-spatial Guidance of Movement during Gesture Imitation and Mirror Drawing in Children with Autism Spectrum Disorders

Thirteen autistic and 14 typically developing children (controls) imitated hand/arm gestures and performed mirror drawing; both tasks assessed ability to reorganize the relationship between spatial goals and the motor commands needed to acquire them. During imitation, children with autism were less accurate than controls in replicating hand shape, hand orientation, and number of constituent limb movements. During shape tracing, children with autism performed accurately with direct visual feedback, but when viewing their hand in a mirror, some children with autism generated fewer errors than controls whereas others performed much worse. Large mirror drawing errors correlated with hand orientation and hand shape errors in imitation, suggesting that visuospatial information processing deficits may contribute importantly to functional motor coordination deficits in autism

Action execution and recognition: a neuropsychological analysis

Humans appear to show an innate tendency to imitate, and this may provide one of the foundations of social communication. Several studies have been carried out in social and cognitive science in order to understand how imitation works, which parts of the brain are involved, and what the role of imitation might be in social behaviour. Previous brain imaging and neuropsychological studies report data that favour a dual process account of imitation, according to which actions are imitated through different mechanisms on the basis of whether they are meaningful and familiar (MF actions) or meaningless/unfamiliar (ML actions). However many questions remain to be clarified – such as which brain areas mediate these different actions. In addition to the distinction between MF and ML gestures, there is considerable interest in the production of different types of known gestures – particularly between actions involving tools (i.e. transitive actions) and those subserving communicative (intransitive) gestures, and in how the production of these gestures relates to the processes involved in recognizing the gestures as input. This thesis reports a neuropsychological examination of the functional and neural bases of imitation using converging data from behavioural studies with different patient groups (stroke patients, patients with Parkinson’s Disease, PD) and structural brain imaging (particularly using voxel-based morphometric [VBM] analyses) to examine lesion-symptom relations. The first empirical chapter (Chapter 2) describes a neuropsychological study on the recognition and production of MF actions and the imitation of ML gestures, in patients with unilateral left or rightside brain damage (respectively: LBD and RBD patients). At a group level, LBD patient were worse in imitation than RBD patients only when novel transitive actions had to be reproduced, when both LBD and RBD differed from healthy participants, while intransitive gestures were generally easier to be executed. Also both transitive and intransitive action imitation tasks were correlated to action recognition. At a single subject level, however, there was evidence for some dissociated symptoms, suggesting that at least partially different mechanisms mediate the imitation of transitive and intransitive gestures and gesture production as opposed to recognition. Chapter 3 presents a first attempt to use VBM to evaluate the relations between brain lesions and the symptoms of apraxia, contrasting the imitation of meaningful (familiar) and meaningless (unfamiliar) transitive and intransitive actions in a consecutive series of brain damaged patients. Chapters 4 and 5 describe two investigations where VBM was again used in a large-scale lesionsymptom analysis of deficits in i) the recognition and generation to command of MF actions and the imitation of ML actions, and ii) the generation to command of different types of learned action (transitive or intransitive gestures). All three investigations using VBM revealed common and differential neural substrates involved in the execution of the tasks considered, and the data are compatible with a model which posits that different processes are involved in MF and ML action execution, as well as in action understanding. The results also suggest that the distinction between transitive and intransitive actions may be included in an action reproduction system. In the final empirical chapter (Chapter 6), I report a study on PD patients tested for imitation of transitive and intransitive MF and ML actions, also relating their performance to the neurological/peripheral symptoms of the disease. This study revealed that PD patients were impaired in imitation, and they also had different pattern of deficit for transitive and intransitive actions. The correlation with peripheral symptoms was not significant, though there were correlations with underlying cognitive processes likely to support action production. Chapter 7 summarizes the different results and links them back to functional and neural accounts of action recognition, production and imitation. The relations between action production and recognition and other cognitive processes are discussed, as are methodological issues concerning lesion-symptom mapping

Repetitive transcranial magnetic stimulation reveals a role for the left inferior parietal lobule in matching observed kinematics during imitation

Apraxia (a disorder of complex movement) suggests that the left inferior parietal lobule plays a role in kinematic or spatial aspects of imitation, which may be particularly important for meaningless (i.e., unfamiliar intransitive) actions. Mirror neuron theories indicate that the inferior parietal lobule is part of a frontoparietal system that can support imitation by linking observed and stored actions through visuomotor matching, and have less to say about different subregions of the left inferior parietal lobule, or how different types of action (i.e., meaningful or meaningless) are processed for imitation. We used repetitive transcranial magnetic stimulation (rTMS) to bridge this gap and better understand the roles of the left supramarginal gyrus and left angular gyrus in imitation. We also examined if these areas are differentially involved in meaningful and meaningless action imitation. We applied rTMS over the left supramarginal gyrus, left angular gyrus, or during a no-rTMS baseline condition, then asked participants to imitate a confederate’s actions whilst the arm and hand movements of both individuals were motion-tracked. rTMS over both the left supramarginal gyrus and the left angular gyrus reduced the velocity of participants' finger movements relative to the actor during imitation of finger gestures, regardless of action meaning. Our results support recent claims in apraxia and confirm a role for the left inferior parietal lobule in kinematic processing during gesture imitation, regardless of action meaning

Selective imitation impairments differentially interact with language processing

Whether motor and linguistic representations of actions share common neural structures has recently been the focus of an animated debate in cognitive neuroscience. Group studies with brain-damaged patients reported association patterns of praxic and linguistic deficits whereas single case studies documented double dissociations between the correct execution of gestures and their comprehension in verbal contexts. When the relationship between language and imitation was investigated, each ability was analysed as a unique process without distinguishing between possible subprocesses. However, recent cognitive models can be successfully used to account for these inconsistencies in the extant literature. In the present study, in 57 patients with left brain damage, we tested whether a deficit at imitating either meaningful or meaningless gestures differentially impinges on three distinct linguistic abilities (comprehension, naming and repetition). Based on the dual-pathway models, we predicted that praxic and linguistic performance would be associated when meaningful gestures are processed, and would dissociate for meaningless gestures. We used partial correlations to assess the association between patients' scores while accounting for potential confounding effects of aspecific factors such age, education and lesion size. We found that imitation of meaningful gestures significantly correlated with patients' performance on naming and repetition (but not on comprehension). This was not the case for the imitation of meaningless gestures. Moreover, voxel-based lesion-symptom mapping analysis revealed that damage to the angular gyrus specifically affected imitation of meaningless gestures, independent of patients' performance on linguistic tests. Instead, damage to the supramarginal gyrus affected not only imitation of meaningful gestures, but also patients' performance on naming and repetition. Our findings clarify the apparent conflict between associations and dissociations patterns previously observed in neuropsychological studies, and suggest that motor experience and language can interact when the two domains conceptually overla

Neural correlates of transitive and intransitive action imitation:an investigation using voxel-based morphometry

AbstractThe ability to reproduce visually presented actions has been studied through neuropsychological observations of patients with ideomotor apraxia. These studies include attempts to understand the neural basis of action reproduction based on lesion–symptom mapping in different patient groups. While there is a convergence of evidence that areas in the parietal and frontal lobes within the left hemisphere are involved in the imitation of a variety of actions, questions remain about whether the results generalize beyond the imitation of tool use and whether the presence of a strong grasp component of the action is critical. Here we used voxel-based lesion–symptom mapping to assess the neural substrates of imitating meaningful (familiar, MF) and meaningless (unfamiliar, ML) tool-related (transitive) and non-tool related (intransitive) actions. The analysis showed that the left parietal cortex was involved in the imitation of transitive gestures, regardless of whether they were meaningful or not. In addition there was poor reproduction of meaningless actions (both transitive and intransitive) following damage of the right frontal cortex. These findings suggest a role of right frontal regions in processing of unfamiliar actions

Neural correlates of the processing of co-speech gestures

In communicative situations, speech is often accompanied by gestures. For example, speakers tend to illustrate certain contents of speech by means of iconic gestures which are hand movements that bear a formal relationship to the contents of speech. The meaning of an iconic gesture is determined both by its form as well as the speech context in which it is performed. Thus, gesture and speech interact in comprehension. Using fMRI, the present study investigated what brain areas are involved in this interaction process. Participants watched videos in which sentences containing an ambiguous word (e.g. She touched the mouse) were accompanied by either a meaningless grooming movement, a gesture supporting the more frequent dominant meaning (e.g. animal) or a gesture supporting the less frequent subordinate meaning (e.g. computer device). We hypothesized that brain areas involved in the interaction of gesture and speech would show greater activation to gesture-supported sentences as compared to sentences accompanied by a meaningless grooming movement. The main results are that when contrasted with grooming, both types of gestures (dominant and subordinate) activated an array of brain regions consisting of the left posterior superior temporal sulcus (STS), the inferior parietal lobule bilaterally and the ventral precentral sulcus bilaterally. Given the crucial role of the STS in audiovisual integration processes, this activation might reflect the interaction between the meaning of gesture and the ambiguous sentence. The activations in inferior frontal and inferior parietal regions may reflect a mechanism of determining the goal of co-speech hand movements through an observation-execution matching process

Semantics in the Motor System: Motor-Cortical Beta Oscillations Reflect Semantic Knowledge of End-Postures for Object Use

In the present EEG study we investigated whether semantic knowledge for object use is represented in motor-related brain areas. Subjects were required to perform actions with everyday objects and to maintain either a meaningful or a meaningless end posture with the object. Analysis of the EEG data focused on the beta-frequency band, as previous studies have indicated that the maintenance of a posture is reflected in stronger beta-oscillations. Time frequency analysis indicated that the execution of actions resulting in a meaningless compared to a meaningful end posture was accompanied by a stronger beta-desynchronization towards the end of the movement and a stronger subsequent beta-rebound after posture-onset. The effect in the beta-frequency band was localized to premotor, parietal and medial frontal areas and could not be attributed to differences in timing or movement complexity between meaningful and meaningless actions. Together these findings directly show that the motor system is differentially activated during the execution and maintenance of semantically correct or incorrect end postures. This suggests that semantic object knowledge is indeed represented in motor-related brain areas, organized around specific end postures associated with the use of objects

Action observation and execution: What is shared?

Performing an action and observing it activate the same internal representations of action. The representations are therefore shared between self and other (shared representations of action, SRA). But what exactly is shared? At what level within the hierarchical structure of the motor system do SRA occur? Understanding the content of SRA is important in order to decide what theoretical work SRA can perform. In this paper, we provide some conceptual clarification by raising three main questions: (i) are SRA semantic or pragmatic representations of action?; (ii) are SRA sensory or motor representations?; (iii) are SRA representations of the action as a global unit or as a set of elementary motor components? After outlining a model of the motor hierarchy, we conclude that the best candidate for SRA is intentions in action, defined as the motor plans of the dynamic sequence of movements. We shed new light on SRA by highlighting the causal efficacy of intentions in action. This in turn explains phenomena such as inhibition of imitation