Alessia Tessari

Common and Differential Neural Mechanisms Supporting Imitation of Meaningful and Meaningless Actions

Neuropsychological studies indicate that, after brain damage, the ability to imitate meaningful or meaningless actions can be selectively impaired. However, the neural bases supporting the imitation of these two types of action are still poorly understood. Using PET, we investigated in 10 healthy individuals the neural mechanisms of imitating novel, meaningless actions and familiar, meaningful actions. Data were analyzed using SPM99. During imitation, a significant positive correlation (p < .05, corrected) of regional cerebral blood flow with the amount of meaningful actions was observed in the left inferior temporal gyrus only. In contrast, a significant positive correlation (p < .05, corrected) with the amount of meaningless movements was observed in the right parieto-occipital junction. The direct categorical comparison of imitating meaningful (100) relative to meaningless (100) actions showed differential increases in neural activity (p < .001, uncorrected) in the left inferior temporal gyrus, the left parahippocampal gyrus, and the left angular gyrus. The reverse categorical comparison of imitating meaningless (100) relative to meaningful (100) actions revealed differential increases in neural activity (p < .001, uncorrected) in the superior parietal cortex bilaterally, in the right parieto-occipital junction, in the right occipital-temporal junction (MT, V5), and in the left superior temporal gyrus. Increased neural activity common to imitation of meaningless and meaningful actions compared to action observation was observed in a network of areas known to be involved in imitation of actions including the primary sensorimotor cortex, the supplementary motor area, and the ventral premotor cortex. These results are compatible with the two-route model of action imitation which suggests that there are at least two mechanisms involved in imitation of actions: a direct mechanism transforming a novel action into a motor output, and a semantic mechanism, on the basis of stored memories, that allows reproductions of known actions. Our results indicate that, in addition to shared neural processes, the direct and the semantic mechanisms that underlie action imitation also draw upon differential neural mechanisms. The direct mechanism underlying imitation of meaningless actions differentially involves visuospatial transformation processes as evidenced by activation of areas belonging to the dorsal stream. In contrast, imitation of meaningful actions differentially involves semantic processing as evidenced by activation of areas belonging to the ventral stream.

The strategic control of multiple routes in imitation of actions.

The aim of this study was to bring to the surface the strategic use of imitative processes in the context of a 2-route model: (a) direct imitation, used in reproducing new, meaningless actions, and (b) imitation based on stored semantic knowledge of familiar meaningful actions. Three experiments were carried out with healthy participants who reproduced meaningful and meaningless actions within an established time limit. The study investigated 3 factors that could potentially affect the selection of processes used for imitation: (a) the composition of the experimental list (blocked or mixed presentation), (b) the presence-absence of instructions (Experiments 1 and 2), and (c) the relative proportions of the stimuli (Experiment 3). Overall, the results suggest that each of these factors influences the selection of imitative strategies in healthy individuals with temporarily reduced capacities, as happens in the case of brain-damaged patients.

Imitation of novel and well-known actions: the role of short-term memory.

Abstract. Four experiments were carried out using the action span paradigm. In experiment 1 we found that well-learnt, meaningful (MF) actions were imitated better than novel, meaningless (ML) actions. In experiments 2 and 3, during the encoding of MF and ML actions, participants were required to carry out different suppression tasks. In experiment 2 we replicated the advantage of MF actions over ML actions and also found that the motor suppression shortened the action span more than the other forms of suppressions (spatial and articulatory). Action encoding and motor suppression tapping the same subsystem, temporarily holding the motor information, could explain the reduced motor span obtained in experiment 2. Two alternative explanations that could have accounted for this effect were ruled out in experiments 3 and 4. In experiment 3 we verified whether the reduction of the action span was produced by the different combination of the articulatory suppression with motor suppression or with the spatial suppression. In experiment 4, we demonstrated that the reduction was not due to the motor suppression being more difficult than the other types of suppression. The critical finding that the spans of well-learnt, MF actions are longer than those of novel, ML actions observed in experiments 1 and 2 was interpreted in terms of different processing routes engaged in the imitation of these two types of actions. MF actions can be imitated along both a semantic, indirect route and a direct route leading from the visual analysis of the action to the motor system. In contrast, the imitation of ML actions is accomplished along the direct route only.

Imitation of novel and well-known actions

Four experiments were carried out using the action span paradigm. In experiment 1 we found that well-learnt, meaningful (MF) actions were imitated better than novel, meaningless (ML) actions. In experiments 2 and 3, during the encoding of MF and ML actions, participants were required to carry out different suppression tasks. In experiment 2 we replicated the advantage of MF actions over ML actions and also found that the motor suppression shortened the action span more than the other forms of suppressions (spatial and articulatory). Action encoding and motor suppression tapping the same subsystem, temporarily holding the motor information, could explain the reduced motor span obtained in experiment 2. Two alternative explanations that could have accounted for this effect were ruled out in experiments 3 and 4. In experiment 3 we verified whether the reduction of the action span was produced by the different combination of the articulatory suppression with motor suppression or with the spatial suppression. In experiment 4, we demonstrated that the reduction was not due to the motor suppression being more difficult than the other types of suppression. The critical finding that the spans of well-learnt, MF actions are longer than those of novel, ML actions observed in experiments 1 and 2 was interpreted in terms of different processing routes engaged in the imitation of these two types of actions. MF actions can be imitated along both a semantic, indirect route and a direct route leading from the visual analysis of the action to the motor system. In contrast, the imitation of ML actions is accomplished along the direct route only.

Abstract and Concrete Phrases Processing Differentially Modulates Cortico-Spinal Excitability

An important challenge of embodied theories is to explain the comprehension of abstract sentences. The aim of the present study was to scrutinize the role of the motor cortex in this process. We developed a new paradigm to study the abstract-concrete dimension by combining concrete (i.e., action-related) and abstract (i.e., non-action-related) verbs with nouns of graspable and non-graspable objects. Using these verb-noun combinations we performed a Transcranial Magnetic Stimulation (TMS) on the left primary motor cortex while participants performed a sentence sensibility task. Single-TMS pulses were delivered 250ms after verb or noun presentation in each of four combinations of abstract and concrete verbs and nouns. To evaluate cortico-spinal excitability we registered the electromyographic activity of the right first dorsal interosseous muscle. As to verb-noun integration, analysis of motor evoked potentials (MEPs) after TMS pulse during noun presentation revealed greater peak-to-peak amplitude in phrases containing abstract rather than concrete verbs. Response times were also collected and showed that compatible (Concrete-Concrete and Abstract-Abstract) combinations were processed faster than mixed ones; moreover in combinations containing concrete verbs, participants were faster when the pulse was delivered on the first word (verb) than on the second one (noun). Results support previous findings showing early activation of hand-related areas after concrete verbs processing. The prolonged or delayed activation of the same areas by abstract verbs will be discussed in the framework of recent embodied theories based on multiple types of representation, particularly theories emphasizing the role of different acquisition mechanisms for concrete and abstract words (Borghi and Cimatti, 2009,2012).

When motor attention improves selective attention: The dissociating role of saliency

There is evidence that preparing and maintaining a motor plan (“motor attention”) can bias visual selective attention. For example, a motor attended grasp biases visual attention to select appropriately graspable object features (Symes, Tucker, Ellis, Vainio, & Ottoboni, 2008). According to the biased competition model of selective attention, the relative weightings of stimulus-driven and goal-directed factors determine selection. The current study investigated how the goal-directed bias of motor attention might operate when the stimulus-driven salience of the target was varied. Using a change detection task, two almost identical photographed scenes of simplistic graspable objects were presented flickering back and forth. The target object changed visually, and this change was either high or low salience. Target salience determined whether or not the motor attended grasp significantly biased visual selective attention. Specifically, motor attention only had a reliable influence on target detection times when the visual salience of the target was low.

Effect of learning on imitation of new actions: implications for a memory model

The effects of learning on strategy selection in the context of action imitation have been investigated in two experiments conducted with healthy individuals. It was predicted that, once learnt, meaningless actions are processed by the cognitive system as meaningful and this new representational status might influence the process selection in action imitation. Results showed that not only were learnt meaningless actions processed in the same way as known, meaningful actions, but that they were imitated even better, probably due to their being represented only once in the episodic, long-term memory system. Our findings are interpreted in the light of a multiple route model for action imitation.

Motor distal component and pragmatic representation of objects.

In this study, we tested whether in certain experimental conditions the distal and proximal motor components may dissociate in action imitation, and how the distal component and the object representation may interact. Experiments 1-3 were carried out using a dual task procedure in which an action span and a motor suppression were coupled. In Experiment 1, it was shown that action spans were affected more by a distal movement (e.g. distal motor suppression) than by a proximal movement (proximal motor suppression). In Experiment 2, it was demonstrated that the reduction of the action spans was not due to the distal motor suppression being more difficult than the proximal motor suppression. In Experiment 3, pantomimes were replaced with the corresponding objects and the participants were asked to mime the objects, reproducing the appropriate actions. During the presentation of the objects, the participants were engaged in a motor suppression that was performed either by the hand or by the arm. The distal motor suppression reduced the pantomime span more significantly than the proximal motor suppression. Experiment 4 showed that the spans of pantomimes of objects shown in Experiment 3 are longer when participants do not perform motor suppressions. Our results suggest that in normal subjects a difference between the distal and the proximal motor component can be observed under dual task conditions and that distal motor suppression seems to interfere both with the encoding of action and with pragmatic representation of objects.

Is access to the body structural description sensitive to a body part’s significance for action and cognition? A study of the sidedness effect using feet

There is evidence suggesting that viewing hands triggers automatic access to the Body Structural Description, a visual-spatial representation of human body parts configuration. Hands, however, have a special representational status within the brain because of their significance for action and cognition. We tested whether feet, less important in gestural and object-directed action, would similarly show automatic access to the Body Structural Description. Positive evidence of that would be finding a Sidedness effect (Ottoboni et al. J Exp Psychol Hum Percept Perform 31:778–789, 2005), a Simon-like paradigm previously used to study automatic hand recognition. This effect demonstrates that processing hands generates spatial codes corresponding to the side of the body on which the hand would be located within the Body Structural Description map. Feet were shown with toes pointing upwards (Experiment 1), without any connection to the ankle and the leg (Experiment 2) and with toes pointing downwards (Experiment 3). Results revealed a Sidedness effect in both Experiments 1 and 3: spatial compatibility occurred according to the side of the body that each foot would assume within the Body Structural Description. In Experiment 2, as already found in stimuli similarly featured, no effect emerged, due to the lack of the necessary anatomical links connecting the foot to a body. Results suggest that body parts with variable degrees of significance for action and cognition can access automatically the Body Structural Description hence reinforcing the hypothesis of its pure visuo-spatial nature.

Modulation of the affordance effect through transfer of learning.

Consistent evidence shows that practising with spatially incompatible stimulus–response trials modulates performance on following tasks requiring the solution of cognitive conflict such as the Simon and Stroop tasks. In the present study we assessed whether a spatially incompatible practice can modulate another effect that is thought to be due to a conflict between two response alternatives, the affordance effect. To this end, we requested participants to categorize pictures of common objects on the basis of their upright or inverted orientation. A group of participants performed the categorization task alone, while the other two groups performed the categorization task after practising with a spatial compatibility task with either a compatible or an incompatible mapping. Results showed that the spatially incompatible practice eliminated the affordance effect. These results indicate that the conflict at the basis of the affordance effect is not unavoidable but it rather permeable to modulations affecting the response selection stage. Indeed the “emit the alternative spatial response” rule acquired during the spatially incompatible task can transfer to and modulate how the subsequent affordance task is performed.