Role-Specific Brain Activations in Leaders and Followers During Joint Action

Much of social interaction in human life requires that individuals perform different roles during joint actions, the most basic distinction being that between a leader and a follower. A number of neuroimaging studies have examined the brain networks for leading and following, but none have examined what effect prior expertise at these roles has on brain activations during joint motor tasks. Couple dancers (e.g., dancers of Tango, Salsa, and swing) are an ideal population in which examine such effects, since leaders and followers of partnered dances have similar overall levels of motor expertise at dancing, but can differ strikingly in their role-specific skill sets. To explore role-specific expertise effects on brain activations for the first time, we recruited nine skilled leaders and nine skilled followers of couple dances for a functional magnetic resonance imaging study. We employed a two-person scanning arrangement that allowed a more naturalistic interaction between two individuals. The dancers interacted physically with an experimenter standing next to the bore of the magnet so as to permit bimanual partnered movements. Together, they alternated between leading and following the joint movements. The results demonstrated that the brain activations during the acts of leading and following were enhanced by prior expertise at being a leader or follower, and that activity in task-specific brain areas tended to be positively correlated with the level of expertise at the corresponding role. These findings provide preliminary evidence that training at one role of a joint motor task can selectively enhance role-related brain activations

Taking two to tango:fMRI analysis of improvised joint action with physical contact

<div><p>Many forms of joint action involve physical coupling between the participants, such as when moving a sofa together or dancing a tango. We report the results of a novel two-person functional MRI study in which trained couple dancers engaged in bimanual contact with an experimenter standing next to the bore of the magnet, and in which the two alternated between being the leader and the follower of joint improvised movements. Leading showed a general pattern of self-orientation, being associated with brain areas involved in motor planning, navigation, sequencing, action monitoring, and error correction. In contrast, following showed a far more sensory, externally-oriented pattern, revealing areas involved in somatosensation, proprioception, motion tracking, social cognition, and outcome monitoring. We also had participants perform a “mutual” condition in which the movement patterns were pre-learned and the roles were symmetric, thereby minimizing any tendency toward either leading or following. The mutual condition showed greater activity in brain areas involved in mentalizing and social reward than did leading or following. Finally, the analysis of improvisation revealed the dual importance of motor-planning and working-memory areas. We discuss these results in terms of theories of both joint action and improvisation.</p></div

Improvisation and self-initiation.

<p>Talairach coordinates for the peak activations and deactivations for the contrast “improvised versus non-improvised” (i.e., Leading + Solo > Mutual + Alone), p < 0.05 with FDR correction. Also included are the coordinates for the peak activations for the contrast “self-initiated versus externally-triggered” ([Leading + Solo + Mutual + Alone] > Following), p < 0.05 with FDR correction. BA = Brodmann area, k = number of voxels, t = maximum t value, RH = right hemisphere, LH = left hemisphere. Abbreviations: CMA, cingulate motor area; DLPFC, dorsolateral prefrontal cortex; IFG, inferior frontal gyrus; M1, primary motor cortex; PHC, parahippocampal gyrus: PMC, premotor cortex; SMA, supplementary motor area; SPL, superior parietal lobule; STG, superior temportal gyrus; TPJ = temporo-parietal junction.</p

Improvisation and self-initiation.

<p>Talairach coordinates for the peak activations and deactivations for the contrast “improvised versus non-improvised” (i.e., Leading + Solo > Mutual + Alone), p < 0.05 with FDR correction. Also included are the coordinates for the peak activations for the contrast “self-initiated versus externally-triggered” ([Leading + Solo + Mutual + Alone] > Following), p < 0.05 with FDR correction. BA = Brodmann area, k = number of voxels, t = maximum t value, RH = right hemisphere, LH = left hemisphere. Abbreviations: CMA, cingulate motor area; DLPFC, dorsolateral prefrontal cortex; IFG, inferior frontal gyrus; M1, primary motor cortex; PHC, parahippocampal gyrus: PMC, premotor cortex; SMA, supplementary motor area; SPL, superior parietal lobule; STG, superior temportal gyrus; TPJ = temporo-parietal junction.</p

Specific activations for Leading, Following, and Mutual.

<p>Talairach coordinates for the peak activations for the contrasts “one partnered condition versus the conjunction of the three partnered conditions” (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0191098#sec002" target="_blank">Methods</a> for details), p < 0.005 uncorrected. BA = Brodmann area, k = number of voxels, t = maximum t value, RH = right hemisphere, LH = left hemisphere. Abbreviations: ACC, anterior cingulate cortex; aIPL, anterior inferior parietal lobule; Amyg., amygdala; CMA, cingulate motor area; IFG, inferior frontal gyrus; M1, primary motor cortex; MFG, medial frontal gyrus; mPFC, medial prefrontal cortex; MT+/V5, motion area of the middle temporal region; PMC, premotor cortex; pSTS, posterior superior temporal sulcus; Put., putamen; S2, secondary somatosensory cortex; SMA, supplementary motor area; SPL, superior parietal lobule; STG, superior temporal gyrus; TPJ, temporo-parietal junction.</p

Joint improvisation.

<p>Talairach coordinates for the peak activations and deactivations for the contrast “Leading > Solo”, p < 0.05 with FDR correction. BA = Brodmann area, k = number of voxels, t = maximum t value, RH = right hemisphere, LH = left hemisphere. Abbreviations: MCC, middle cingulate cortex; S1, primary somatosensory cortex; S2, secondary somatosensory cortex.</p

Specificity for Leading, Following, and Mutual.

<p>Neural specificity for Leading, Following and Mutual is shown, after removing both basic motoric effects (through subtraction of the non-partnered conditions Solo + Alone) and partnering effects, as seen in a conjunction of the three partnership contrasts: [Leading > non-partnered conditions] ∩ [Following > non-partnered conditions] ∩ [Mutual> non-partnered conditions]. The role-specific activations are color-coded as follows: Leading (red): [Leading > Non-partnered conditions] > [Partnership Conjunction]; Following (blue): [Following > Non-partnered conditions] > [Partnership Conjunction]; and Mutual (yellow): [Mutual> Non-partnered conditions] > [Partnership Conjunction]. The results are p < 0.005 uncorrected, with a cluster threshold k = 20. Abbreviations: aIPL: anterior inferior parietal lobule; MCC: middle cingulate cortex; MT+/V5, motion area of the middle temporal region; mPFC: medial prefrontal cortex; NA: nucleus accumbens; pSTS: posterior superior temporal sulcus; S1: primary somatosensory cortex; S2: secondary somatosensory cortex; TPJ: temporo-parietal junction.</p

Effect of improvisation.

<p>(A) Whole-brain analysis of improvisation: Leading + Solo > Mutual + Alone. p < 0.05 FDR corrected with a cluster threshold k = 20. Orange = activation, and blue = deactivation. Based on the results of the ROI analysis presented in panel B, areas with red labels in this panel (and that are surrounded with a red box in panel B) are those that are more likely to be involved in improvisational generation of movement, whereas those areas with green labels (and that are surrounded with a green box in panel B) are more likely to be associated with movement variability, rather than improvisation. Abbreviations: CMA: cingulate motor area; DLPFC: dorsolateral prefrontal cortex; IFG: inferior frontal gyrus; PMC: premotor cortex; SMA: supplementary motor area; SPL: superior parietal lobule; STG: superior temporal gyrus. (B) ROI analysis of the improvisation areas in comparison with the Following condition. ** = p < 0.005, * = p < 0.05, • = trend (p = 0.057). Error bars are standard errors of the mean. Beta weights extracted from spheres of 5 mm radius are centered on the peak of the areas defined in the improvisation contrast in panel A (Leading + Solo > Mutual + Alone). Improvised (red): mean across Leading + Solo. Non-improvised (green): mean across Mutual + Alone. The means are averaged across both hemispheres for the bilateral areas (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0191098#pone.0191098.t003" target="_blank">Table 3</a>).</p

Main effect of partnering.

<p>Partnering was examined by contrasting the partnered conditions with the non-partnered conditions (Leading + Following + Mutual > Solo + Alone), with results reported at p < 0.05, FDR corrected, with a cluster threshold k = 20. The results in Figs <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0191098#pone.0191098.g002" target="_blank">2</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0191098#pone.0191098.g004" target="_blank">4</a> are registered onto a Talairach-normalized anatomical template MRI (the Colin brain). The Talairach z coordinate is shown below each slice. The left side of the slice is the left side of the brain. Abbreviations: MCC: middle cingulate cortex; mPFC: medial prefrontal cortex; pSTS: posterior superior temporal sulcus; S1: primary somatosensory cortex; S2: secondary somatosensory cortex; TPJ: temporo-parietal junction.</p

Partnering.

<p>Talairach coordinates for the peak activations for the contrast “partnered versus non-partnered” (i.e., Leading + Following + Mutual > Solo + Alone), p < 0.05 with FDR correction. BA = Brodmann area, k = number of voxels, t = maximum t value, RH = right hemisphere, LH = left hemisphere. Abbreviations: aIPL, anterior inferior parietal lobule; FG, fusiform gyrus; IFG, inferior frontal gyrus; MCC, middle cingulate cortex; mPFC, medial prefrontal cortex; MT+/V5, motion area of the middle temporal region; S1, primary somatosensory cortex; S2, secondary somatosensory cortex; pSTS, posterior superior temporal sulcus; TPJ = temporo-parietal junction.</p