"The neural correlates of grasping actions:observation and execution"
Year: 2009
Type: dissertation
Abstract: Summary The aim of the present thesis was to shed further light on the properties characterizing the neural system underlying action understanding in humans. This was done in terms of both pure action observation and “mirror” type of activity by means of functional resonance imaging (fMRI). In first instance, I conducted a series of studies in which participants were simply asked to observe a model’s grasping action while their brain was scanned. Here the targeted neural system was the action observation system (AOS), a network of regions automatically recruited during the observation of action performed by others (Buccino et al., 2001). In second instance, the performed experimentation involved the recording of the participants’ neural activity during both the observation and the execution of grasping actions. Here the targeted neural system was the so called “mirror” system (Rizzolatti & Craighero, 2004). To start with, I considered the investigation of the AOS in a population affected by a severe neurological disorder, i.e. early relapsing remitting multiple sclerosis (RRMS) patients (Chapter 3). During scanning, participants simply observed images depicting a human hand either grasping an object or resting alongside an object. Although previous evidence indicates a selective impairment of the AOS in MS patients, the present findings are not suggestive of any specific deficit at the level of this system in these patients. Rather, they showed a general, but unspecific, effect of BOLD over-activation which was probably determined by the extensive demyelination caused by the disease and by the consequent repairing process carried out by our organism. Such unspecific over-activation has been discussed in terms of the spared ability of the AOS to re-enact stored motor representations which might be used for rehabilitating motor control in RRMS (action observation therapy; Ertelt et al., 2007; Buccino, Solodkin, & Small, 2006). In the second experimental chapter (Chapter 4), I focused on a more basic feature of the human AOS, the coding of not-object-related (intransitive) actions. This is a unique feature of the human AOS, because in non-human primates the AOS seems not to code for such types of actions. The central advance of this study is the demonstration that transitivity conveyed by previous knowledge regarding the presence/absence of a target-object modulates activity within the AOS. By manipulating this type of information we revealed that the AOS is able to generate a representation of an observed action on the basis of the action goal, even when the most crucial part of the action (i.e., hand-object interaction) is not visible. A number of studies put forward the proposal that the human AOS responds to intransitive actions (Buccino et al., 2001; Wheaton, Thompson, Syngeniotis, Abbott, & Puce, 2004; Dinstein, Hasson, Rubin, & Heeger, 2007; Dinstein, Gardner, Jazayeri, & Heeger, 2008; Lui, et al., 2008) suggesting that when a target-object is not present the AOS is still recruited. The present study add to this literature revealing that the AOS has the ability to discriminate and understand observed actions on the basis of the properties characterizing their goal (i.e. transitivity) rather than their perceived physical features. In this sense, we were able to find a modulation within the AOS with respect to the transitivity, suggesting that at least part of the system can be extremely selective in terms of processing the abstract properties of the goal characterizing the observed action. The two final experimental Chapters (Chapters 5 and 6) of the present thesis were concerned with the definition/identification of the human “mirror” regions and (if any) of what they code for. In general, the present results support the notion that in humans “mirror” activity spreads across a number of areas which exceeds those classically thought to be part of the ‘mirror’ system (e.g., Raos, Evangeliou, & Savaki, 2007; Gazzola, Rizzolatti, Wicker, & Keysers, 2007; Gazzola & Keysers, 2009; Evangeliou, Raos, Galletti, & Savaki, 2009). Further, a region of interest analysis (ROI) on the putative human mirror region within the premotor cortex indicate that, in contrast to monkeys (Nelissen, Luppino, Vanduffel, Rizzolatti, & Orban, 2005), this region is activated in a similar fashion irrespective of whether the agent's entire body, or only the grasping hand, is seen. Altogether these results are discussed in terms of the possibility that the AOS and the ‘mirror’ systems chiefly represent actions in terms of goals independently by contextual information (Ferrari, Rozzi, & Fogassi, 2005; Gazzola et al., 2007). The idea is that what is represented in the premotor cortex is not bounded to the physical appearance of the agent, but it is a rather abstract representation centred on the goal of the action, independently of what is acting, a human, a robot, or even a tool. The present findings confirm and extend this notion by broadening the several dimensions within which action goals affect the response of the AOS and how such dimensions may vary across species. Indeed on the basis of monkeys fMRI findings using a paradigm similar to ours (Nelissen et al., 2005) differences in action observation activity depending on type of view were expected, at least within premotor and other prefrontal areas. However, in the present study the type of view had little impact at the level of action observation. I suspect that this might be ascribed to the fact that the processing of particular stimulus properties, which in principle should occur in homologue areas, might not be common to both species (Sereno & Tootell, 2005; Orban, Van Essen, & Vanduffel, 2004; Nakahara, Adachi, Osada, & Miyashita, 2007). In this perspective the conclusion would be that in humans the observation of a grasping hand alone (and an object) is sufficient to trigger significant differential activity. This aspect is particularly important because most of the human studies on the mirror neuron system have been conducted with movies zooming into the hand-part of the stimulus. If, as monkeys’ fMRI indicated (Nelissen et al., 2005), this were to cancel out key mirror areas, much of the human literature would have been challenged. The present data, however, show convincingly that this is not the case, at least in humans, and therefore enhance the validity of a large number of studies providing important and novel evidence within this flourishing field of research. References Buccino, G., Binkofski, F., Fink, G.R., Fadiga, L., Fogassi, L., Gallese, V., et al., (2001). Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. European Journal of Neuroscience, 13, 400–404. Buccino, G., Solodkin, A., & Small, S. (2006). Functions of the mirror neuron system: implications for neurorehabilitation. Cognitive and behavioral neurology, 19, 55-63. Dinstein, I., Hasson, U., Rubin, N., & Heeger, D.J. (2007). Brain areas selective for both observed and executed movements. Journal of Neurophysiology, 98, 1415–1427. Dinstein, I., Gardner, J.L., Jazayeri, M. & Heeger, D.J. (2008). Executed and observed movements have different distributed representations in human aIPS. Journal of Neuroscience, 28, 11231–11239. Ertelt, D., Small, S., Solodkin, A., Dettmers, C., McNamara, A., & Buccino, G. (2007). Action observation has a positive impact on rehabilitation of motor deficits after stroke. NeuroImage, 36, T164-173. Evangeliou, M.N., Raos, V., Galletti, C., & Savaki, H.E. (2009). Functional imaging of the parietal cortex during action execution and observation. Cerebral Cortex, 19, 624–639. Ferrari, P.F., Rozzi, S. & Fogassi, L. (2005). Mirror neurons responding to observation of actions made with tools in monkey ventral premotor cortex. Journal of Cognitive Neuroscience, 17, 212-226. Gazzola, V., Rizzolatti, G., Wicker, B. & Keysers, C. (2007). The anthropomorphic brain: The mirror neuron system responds to human and robotic actions. NeuroImage, 35, 1674-1684. Gazzola, V., & Keysers, C. (2009). The observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI data. Cerebral Cortex, 19, 1239-55. Lui, F., Buccino, G., Duzzi, D., Benuzzi, F., Crisi, G., Baraldi, P., et al. (2008). Neural substrates for observing and imagining non-object-directed actions. Social Neuroscience, 3, 261-75. Nakahara, K., Adachi, Y., Osada, T., & Miyashita, Y. (2007). Exploring the neural basis of cognition: multi-modal links between human fMRI and macaque neurophysiology. Trends in Cognitive Sciences, 11, 84–92. Nelissen, K., Luppino, G., Vanduffel, W., Rizzolatti, G., & Orban, G. A. (2005). Observing others: multiple action representation in the frontal lobe. Science, 310, 332-336. Orban, G.A., Van Essen, D., & Vanduffel, W. (2004). Comparative mapping of higher visual areas in monkeys and humans. Trends in Cognitive Sciences, 8, 315–324. Raos, V., Evangeliou, M.N., & Savaki, H.E. (2007). Mental simulation of action in the service of action perception. Journal of Neuroscience, 27, 12675-12683. Rizzolatti, G., Fogassi, L., & Gallese, V. (2001). Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Reviews Neuroscience, 2, 661–670. Sereno, M.I. & Tootell, R.B. (2005). From monkeys to humans: what do we now know about brain homologies? Current Opinion in Neurobiology, 15, 135-144. Wheaton, K.J., Thompson, J.C., Syngeniotis, A., Abbott, D.F., & Puce, A. (2004). Viewing the motion of human body parts activates different regions of premotor, temporal, and parietal cortex. NeuroImage, 22, 277-88.
Author: Luca Turella
Language: English
Subfield: Social Psychology
Field: Psychology
Domain: Social Sciences
Open Access status: green
OpenAlex ID: W121784611