Neural representations involved in observed, imagined, and imitated actions are dissociable and hierarchically organized

Abstract

The fact that action observation, motor imagery and execution are associated with partially overlapping increases in parieto-frontal areas has been interpreted as evidence for reliance of these behaviors on a common system of motor representations. However, studies that include all three conditions within a single paradigm are rare, and consequently, there is a dearth of knowledge concerning the distinct mechanisms involved in these functions. Here we report key differences in neural representations subserving observation, imagery, and synchronous imitation of a repetitive bimanual finger-tapping task using fMRI under conditions in which visual stimulation is carefully controlled. Relative to rest, observation, imagery, and synchronous imitation are all associated with widespread increases in cortical activity. Importantly, when effects of visual stimulation are properly controlled, each of these conditions is found to have its own unique neural signature. Relative to observation or imagery, synchronous imitation shows increased bilateral activity along the central sulcus (extending into precentral and postcentral gyri), in the cerebellum, supplementary motor area (SMA), parietal operculum, and several motor-related subcortical areas. No areas show greater increases for imagery vs. synchronous imitation; however, relative to synchronous imitation, observation is associated with greater increases in caudal SMA activity than synchronous imitation. Compared to observation, imagery increases activation in pre-SMA and left inferior frontal cortex, while no areas show the inverse effect. Region-of-interest (ROI) analyses reveal that areas involved in bimanual open-loop movements respond most to synchronous imitation (primary sensorimotor, classic SMA, and cerebellum), and less vigorously to imagery and observation. The differential activity between conditions suggests an alternative hierarchical model in which these behaviors all rely on partially independent mechanisms.

Simulations

“…Similar findings of neural reactivation of sensory and motor brain areas have been found in other cognitive abilities, for example, spatial working memory (Awh & Jonides, 2001), motor imagery (Munzert, Lorey, & Zentgraf, 2009;Macuga & Frey, 2012), and language (Hauk, Johnsrude, & Pulvermüller, 2004). In conclusion, there is a general trend of reactivating brain areas for perception and action in other cognitive functions.…”

“…At other times, reactivations are triggered automatically by the aspects of the environment, such as when reading action words (Hauk, Johnsrude, & Pulvermüller, 2004). Macuga and Frey (2012) compared three different conditions that differed among other things on their reliance on input from the environment and the body: observation, imagery, and imitation of simple finger movements. Consistent with the reactivation hypothesis they found that …all three conditions were associated with increased bilateral increases in activity within a common set of frontal (premotor, pre-SMA), posterior parietal, superior temporal and primary sensorimotor areas, as well as subcortical (thalamus, putamen) regions traditionally implicated in visually-guided bimanual behavior.…”

“…Consistent with the reactivation hypothesis they found that …all three conditions were associated with increased bilateral increases in activity within a common set of frontal (premotor, pre-SMA), posterior parietal, superior temporal and primary sensorimotor areas, as well as subcortical (thalamus, putamen) regions traditionally implicated in visually-guided bimanual behavior. (Macuga & Frey, 2012, p. 2802 To determine whether any difference in brain activity that could be accounted for by other factors than a simulation of the perceptual stimuli per se, they did further comparisons between the different conditions. Based on the assumption that imagining the finger movements would activate a motor plan and possibly the inhibition of executive structures, they found the following when comparing observation vs. imagary.…”

Brain Activity during the Observation, Imagery, and Execution of Tool Use: An fNIRS/EEG Study

“…Previous studies that compared observation, imagery, and execution have included the measurement of the reaching movements of arms using fMRI [8], the reaching motion of the arm using virtual reality and fNIRS [46], wrist movements using fMRI [47], hand movements using transcranial magnetic stimulation (TMS) [48,49], finger movements using fMRI [7], ankle movements using fMRI [50], and the squatting movements of the lower limbs using the heart and breathing rates as indicators [51]. Each of these studies reported similar results under all three conditions.…”

Cortical activation during executed, imagined, observed, and passive wrist movements in healthy volunteers and stroke patients

“…However, the majority of this literature investigated only one mode of covert movement mode or, at most, compared two modes, usually motor imagery and observation (Clark et al, 2003;Filimon et al, 2007;Iseki et al, 2008;Lui et al, 2008;Macuga and Frey, 2012;Munzert et al, 2008;Piefke et al, 2009;Roosink and Zijdewind, 2010;Wang et al, 2008). Therefore inferences between studies have to be made when comparison between all modes of covert movement is to be conducted.…”