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Conceptual processes with and without sensorimotor experience: what is gained and what is missed?

Final Report Summary - ACTICO (Conceptual processes with and without sensorimotor experience: what is gained and what is missed?)

ACTICO aimed at combining functional neuroimaging (functional magnetic resonance imaging, fMRI), non-invasive brain stimulation (Trascranial Magnetic Stimulation, TMS) and behavioral methodologies, to understand the role of sensorimotor brain structures in the representation of conceptual knowledge of actions. As part of the training, and in compliance with the work plan approved for ACTICO, the fellow has developed an international network of scientific collaborations and has taken part to teaching and supervising activities, as described below.

Description of the work performed since the beginning of the project and main results
With the advent of neuroimaging methodologies, brain structures traditionally implicated in mere motor functions (action planning and execution) have been found to respond during higher-level cognitive tasks, such as word understanding [1]. Word-related motor activity could be a neural signature of the influence of individual bodily (or physical) experience on the way the brain represents knowledge about the world. Thus, this research field approaches the question of whether and how bodily experience interacts with, or shapes human cognition.

The research objectives of ACTICO can be summarized as follows:
1. Study of the brain structures involved in the processing of verbs, a category of stimuli that favors the study of conceptual representation of actions in the brain.
2. Study of the division of labor (i.e. the functional role of each area) and network dynamics across the regions involved in the conceptual understanding of actions and action-words, with the objective to develop a coherent neurobiological model of language-semantics.
3. Analysis of cognitive functions and behavior in “special populations” (i.e. population with lack of motor experience and loss of motor functions) to test directly the relationship between the motor system and conceptual representation of action.

The implementation of the experimental part of the work has been preceded by an extensive critical review of the state of the art of research concerning the relationship between language-semantic processing and motor activity. This work has resulted in two publications, respectively focusing on: a) findings on the recruitment of motor brain structures in language-semantic processing; b) the role of sensory-motor (bodily) experience in the acquisition and representation of action knowledge. The experimental part of the project included: a) a series of studies on healthy adults, for the selection of experimental tasks and materials; b) fMRI research on healthy adults to identify the brain regions associated with the representation of verbs’ meanings and the properties of their neural response; c) repetitive TMS research to examine the behavioral effects of temporary perturbation of brain sites involved in verb processing (as identified in the phase a); d) measurement of pattern of motor response to verb processing. Results from phases b, c and d have laid the foundation for developing and implemented a novel TMS procedure, guided by fMRI results, to assess the network dynamics, that is, the functional relationship among different parts of a brain network involved in the same task (here, non-motor associated regions responsive to word understanding, as identified in b, and the precentral motor cortex). Finally, from the collaboration with international groups, the fellow has developed two studies in which the role of the motor system in higher-level cognition (language and conceptual knowledge) has been addressed in a population with Amyotrophic Lateral Sclerosis (ALS), a degenerative Motor Neurone Disease with prime consequences on the motor brain circuitry and motor functioning, and in very young infants (3-/6-months old) with no experience in the motor articulation of speech sounds.

This research has identified a large network of regions, carrying different information during verb processing. A large part of the left temporal cortex responds to verbs more than to other classes of words (i.e. nouns). Our fMRI results have contributed to unpack the apparently monolithic preference for verbs observed in this part of the brain, showing that different aspects of the cortex are sensitive to different aspects of a verb meaning (e.g. the content: abstract vs. concrete, the implied subject: “me” or another). Moreover, the response profile of a cluster in the temporal cortex suggests representation of general, abstract information that distinguishes the class of verbs (i.e. predicates) from other classes of words. In contrast, the response of motor regions, in the frontal part of the brain, suggests representation of semantic features that distinguish a specific verb (“jumping”) from another verb (“thinking”). Our research has shown that the former type of information (abstract) is necessary to perform any further computation on a stimulus (e.g. to retrieve the specific feature that distinguish the act “jumping” from the act “thinking”): suppression of temporal cortex activity (through TMS) leads to the abolition of the motor cortex responsiveness to words. This result is likely to highlight a general principle of functioning of the human conceptual architecture, where the retrieval of general abstract representation of stimuli is necessary to access to the representation of their specific features. From a methodological viewpoint, the paradigm implemented to study the interaction among brain regions has introduced a new protocol, which takes advantage of a combination of TMS protocols to study functional connectivity (i.e. interaction across brain regions) during higher-level cognitive tasks.

Behavioral research on ALS patients, in collaboration with the International School for Advanced Studies (SISSA) of Trieste has shown that a loss of motor function due to neurological damage can leave unaffected the conceptual representation of action. Yet, this population exhibits a specific impairment in performing non-motor tasks that require processing the low-level features of an action (e.g. the relation among bodily effectors involved in an action as opposed to the representation of the overarching goals of that action). This research highlights that a stimulus can have different levels of representation which can be computed independently from each other. Finally, research on young infants, carried out in collaboration with the Harvard Baby Lab has investigated the infants’ ability to categorize different speech sounds. The results have shown that, at 6 months, infants succeed in this task despite the fact that they have not yet developed the ability to produce the same sounds with their own vocal tract.

Reference
1. Rumiati RI, Papeo L, Corradi-Dell’Acqua C (2010). Higher-level motor processes. Annals of the New York Academy of Sciences, 1191: 219-241.