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, 37 (4), 1315-28

Human Cortical Representations for Reaching: Mirror Neurons for Execution, Observation, and Imagery

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Human Cortical Representations for Reaching: Mirror Neurons for Execution, Observation, and Imagery

Flavia Filimon et al. Neuroimage.

Abstract

We used functional magnetic resonance imaging (fMRI) to map the cortical representations of executed reaching, observed reaching, and imagined reaching in humans. Whereas previous studies have mostly examined hand actions related to grasping, hand-object interactions, or local finger movements, here we were interested in reaching only (i.e. the transport phase of the hand to a particular location in space), without grasping. We hypothesized that mirror neuron areas specific to reaching-related representations would be active in all three conditions. An overlap between executed, observed, and imagined reaching activations was found in dorsal premotor cortex as well as in the superior parietal lobe and the intraparietal sulcus, in accord with our hypothesis. Activations for observed reaching were more dorsal than activations typically reported in the literature for observation of hand-object interactions (grasping). Our results suggest that the mirror neuron system is specific to the type of hand action performed, and that these fronto-parietal activations are a putative human homologue of the neural circuits underlying reaching in macaques. The parietal activations reported here for executed, imagined, and observed reaching are also consistent with previous functional imaging studies on planned reaching and delayed pointing movements, and extend the proposed localization of human reach-related brain areas to observation as well as imagery of reaching.

Figures

Figure 1
Figure 1
Stimuli used in the experiment. a) The four shapes used as visual stimuli. Each shape was photographed from five different angles, yielding a total of twenty stimulus images. b) Still frame from the observation of reaching video, used in the observed reaching condition. A human hand is seen reaching towards one of the shapes. c) Example trial during either executed or imagined reaching, or passive viewing of objects (baseline). The subject’s task was indicated beforehand with a message.
Figure 2
Figure 2
Group surface-averaged activations for executed, observed, and imagined reaching, versus baseline, from 15 subjects, interpolated onto a single subject’s inflated hemisphere, viewed here from dorsal, posterior, lateral, and medial views. All activations displayed are significant at p<0.005 (corrected). Note the overlap in activations in superior parietal and dorsal premotor cortex (superior frontal gyrus and sulcus), for all three conditions, suggesting the presence of mirror neurons in those areas.
Figure 3
Figure 3
BOLD activations for executed, observed, and imagined reaching, versus baseline, from five representative subjects. Activations are displayed on the left inflated hemisphere of each subject. Each subject’s activations are significant at p < 0.0001. Note that, despite intersubject variability, each subject shows overlap in activations between all three conditions in dorsal premotor and superior parietal cortex. IPS = intraparietal sulcus.
Figure 4
Figure 4
Outline of overlap between executed, observed, and imagined reaching in left dorsal premotor (superior frontal sulcus and gyrus) and left posterior parietal areas, on group surface-averaged activations from 15 subjects, displayed on one subject’s inflated hemisphere. The overlaps in premotor and parietal regions served as regions of interest in the percent signal change analysis. a) Dorsal view of left hemisphere. b) Medial view of left hemisphere. Executed, observed, and imagined reaching all activated a medial parietal area located in-between the parieto-occipital sulcus and the posterior end of the cingulate sulcus, outlined in light blue. Sup. frontal gyr. = superior frontal gyrus; POS = parieto-occipital sulcus; calcarine = calcarine sulcus; cingulate sulc. = cingulate sulcus.
Figure 5
Figure 5
Time course and percent signal change for parietal and premotor regions of interest (ROIs). a) Parietal time course of BOLD signal change during executed, observed, and imagined reaching, versus baseline, averaged over 15 subjects. b) Average parietal percent signal change magnitude for reaching, observed reaching, and imagined reaching, over 15 subjects. Error bars represent standard error of the mean (* p < 0.05). c) Average premotor BOLD time course, as in a), over 15 subjects. d) Average premotor percent signal change magnitude over 15 subjects, for executed, observed, and imagined reaching, as in b). Reaching activations were stronger than observed and imagined reaching activations in both parietal and premotor ROIs.
Figure 6
Figure 6
Comparisons between executed and observed reaching, executed and imagined reaching, and observed versus imagined reaching. Activations are group surface-averages from 15 subjects displayed on a single subject’s inflated left and right hemispheres, p < 0.005 (corrected). Red to bright yellow codes for greater activation for the condition subtracted from. Blue activations represent greater activation for the subtracted condition. Note the lack of difference in premotor and parietal cortex for the observed versus imagined reaching comparison, suggesting that parietal and premotor mirror neurons participate equally in observation and imagery of reaching. IPS = intraparietal sulcus; calcarine = calcarine sulcus; sup. frontal sulcus = superior frontal sulcus; POS = parieto-occipital sulcus; STS = superior temporal sulcus.

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