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. 2012 Feb 1;59(3):2798-807.
doi: 10.1016/j.neuroimage.2011.09.083. Epub 2011 Oct 8.

Neural Representations Involved in Observed, Imagined, and Imitated Actions Are Dissociable and Hierarchically Organized

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Free PMC article

Neural Representations Involved in Observed, Imagined, and Imitated Actions Are Dissociable and Hierarchically Organized

Kristen L Macuga et al. Neuroimage. .
Free PMC article

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.

Figures

Figure 1
Figure 1. Illustration of experimental timeline with representative blocks (not all conditions are displayed)
There were 6 conditions in a 3 (task) × 2 (perspective) design. Verbal presentation of the word “Watch” (Observe), “Imagine” (Imagine), or “Imitate” (Imitate) distinguished conditions 2s prior to each block. Observe from the 1st-person perspective and Imagine from the 3rd-person perspective are shown here for illustrative purposes. Fixation circle always present at the center of the screen. Numbers in thought bubbles illustrate participant’s running count of the number of times the fixation changed from red to blue coincident with the pinkie finger contacting the thumb. Finger tapping was sequential and ‘…’ symbols indicate skipped taps for illustration purposes. See Figure 2 for results verifying task compliance measured by this attentional control.
Figure 2
Figure 2. Behavioral results for orienting task designed to control for variations in attention across conditions
Note that the ordering of runs on the x-axis by number of target changes is done for the purpose of analysis, but does not reflect the actual order of presentation. The run order was counterbalanced across participants. The y-axis refers to the number of fixation changes that occurred during pinkie taps, that participants had to report after completing each run. Mean performance = 88% accuracy, but participants generally underestimated the actual number of fixation color changes during pinkie taps by a mean difference of −2.8, t(55) = 6.83, p < .001, and this underestimation was amplified as the actual number of changes increased.
Figure 3
Figure 3. Conjunction
Common areas of significantly increased activity (vs. resting baseline) for the Observe, the Imagine, AND the Imitate conditions. Here, and in all subsequent figures, we refer to synchronous imitation as “imitation.” Note expected overlap in bilateral frontal (premotor, pre-SMA), posterior parietal, superior temporal and primary sensorimotor areas, as well as subcortical (thalamus, putamen) areas often detected in previous studies of action observation, imagery, and/or execution. Data here and in subsequent figures are displayed on a partially inflated view of CARET’s population-average, landmark- and surface-based (PALS) human brain atlas (ref) (see Methods). Likewise, data in the lower portion of each panel are rendered on axial slices from the group average anatomical image and oriented neurologically.
Figure 4
Figure 4. Areas showing increased activity for the Imitate vs. Observe comparison
In this and subsequent figures, group statistical parametric maps were thresholded at Z>3.1 (corrected clusterwise significance threshold p<0.05). Bilateral precentral and postcentral gyri, cerebellum, SMA, and insula extending into parietal operculum, as well as subcortical structures such as putamen, thalamus, and basal ganglia showed greater responses during imitation vs. observation of actions.
Figure 5
Figure 5. A) Area showing increased activity for the Observe vs. Imitate comparison and B) the calculated mean percent signal change for all 3 conditions in this region
The caudal-most sector of SMA was activated to a significantly greater extent during observation vs. synchronous imitation of actions. We probed this unexpected finding further to make sure that it was not the result of a deactivation in one or more conditions. Instead, we found that in this region, observation and imagery show increases in activation that are significantly greater than synchronous imitation, which does not differ from the resting baseline. Bars represent standard errors.
Figure 6
Figure 6. Areas showing increased activity for the Imitate vs. Imagine comparison
Bilateral precentral and postcentral gyri, cerebellum, SMA, and insula extending into parietal operculum, as well as subcortical structures such as putamen, thalamus, and basal ganglia showed greater responses for imitation vs. imagery of actions.
Figure 7
Figure 7. Areas showing increased activity for the Imagine vs. Observe comparison
Pre-SMA, cingulate, insula, and left inferior frontal cortex were activated to a significantly greater extent during imagery vs. observation of actions.
Figure 8
Figure 8. Percent signal change from the resting baseline within four ROIs: A) left sensorimotor, B) right sensorimotor, C) SMA, and D) cerebellum, shown for all experimental conditions
These were identified by the sensorimotor localizer for execution of the TFST without vision. Bars represent standard errors. All conditions showed activations higher than the resting baseline, with the exception of the observation condition in the cerebellum. Synchronous imitation resulted in greater activity than observation for all ROIs. Imagery and observation showed similar activations in left and right sensorimotor areas, although there was also a marginally significant difference between imagery and observation on the left side. However, in SMA and cerebellum, imagery showed higher activations compared to observation.
Figure 9
Figure 9. Effect of stimulus perspective only in occipital cortex
Data were averaged across Observe, Imagine, and Imitate conditions. Warm colors denote areas more active for 3rd- vs. 1st-person perspective. Cool colors denote areas more active for the 1st- vs. 3rd-person perspective. Effects of the visual perspective manipulation were only seen in occipital areas. As would be expected, the upper visual field (where 3rd person perspective stimulus was displayed) is represented below the calcarine sulcus, and the lower visual field (where 1st person perspective was displayed) is represented. Regions identified by the sensorimotor localizer, however, were perspective invariant.

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