Degeneracy and Complexity in Neuro-Behavioral Correlates of Team Coordination

Abstract

Team coordination-members of a group acting together rather than performing specific actions individually-is essential for success in many real-world tasks such as military missions, sports, workplace, or school interactions. However, team coordination is highly variable, which is one reason why its underlying neural processes are largely unknown. Here we used dual electroencephalography (EEG) in dyads to study the neurobehavioral dynamics of team coordination in an ecologically valid task that places intensive demands on joint performance. We present a novel conceptual framework to interpret neurobehavioral variability in terms of degeneracy, a fundamental property of complex biological systems said to enhance flexibility and robustness. We characterize degeneracy conceptually in terms of a manifold representing the geometric locus of the dynamics in the high dimensional state-space of neurobehavioral signals. The geometry and dimensionality of the manifold are determined by task constraints and team coordination requirements which restrict the manifold to trajectories that are conducive to successful task performance. Our results indicate that team coordination is associated with dimensionality reduction of the manifold as evident in increased inter-brain phase coherence of beta and gamma rhythms during critical phases of task performance where subjects exchange information. Team coordination was also found to affect the shape of the manifold manifested as a symmetry breaking of centro-parietal wavelet power patterns across subjects in trials with high team coordination. These results open a conceptual and empirical path to identifying the mechanisms underlying team performance in complex tasks.

Keywords: coherence; degeneracy; hyperscanning; manifold; social coordination; symmetry breaking; team work; wavelets.

Figure 1

Degeneracy and the geometrical description of behavior. (A) Human dyad engaged in the virtual room clearing task (B) Behavioral degeneracy: Two qualitatively different entry patterns: Leader cross-over (left) and leader button-hook (right). Leader (green) and follower (blue). Both entry patterns are valid forms of task execution. (C) Illustration of the degeneracy of the entry pattern in a 2-D state space comprised of the horizontal locations of the leader and follower, respectively. In the cross-over entry the leader's horizontal location (x-axis) increases while the follower's horizontal location (y-axis) first increases and then decreases (red curve). The converse is the case for the button-hook entry (blue curve) (D) Geometrical description of a behavior as a trajectory in a high-dimensional state space visualized as 3-dimensional space. (E) Degeneracy leads to an ensemble of potential behavioral trajectories which together form a manifold. The 3D manifold (colored surface) and three sample trajectories (red tracks) illustrate the concept. Note that in most cases the behavioral state space has a dimension greater than three and therefore the behavioral manifold cannot be easily visualized. In our case the behavioral state-space of the avatars is 4-dimensional (2-D coordinates of the two avatars) or 6-dimensional, if the respective pieing angles of the two avatars are taken into account as well.

Figure 2

Geometrical framework to formalize degeneracy in behavioral and brain dynamics. The manifolds are represented by the colored surfaces in a 3D state-space (reduced for visualization). All trajectories live on those manifolds, and three exemplars are indicated by the doted lines colored pink, black, and blue, each corresponding to different behavioral dynamics, respectively, but at the same level of team performance, hence lying on the same behavioral manifold. The same behavior can be represented by different neural dynamics, hence on the brain dynamics manifold there are different instances of neural dynamics for each behavioral trajectory.

Figure 3

(A) Inter-brain coherences in the β and γ range that are significantly correlated with leader readiness and (B) corresponding spatial view on an exemplary behavioral sequence. Behavioral sequences in each trial include: Alignment of follower to leader (orange, segment s9, see Tognoli et al., 2011a), preparation to tap (pink, s0), tap (red, s1), movement onset leader (yellow, s2), dyad movement to door (green, s3), entry (blue, s4), movement to corners of dominance. (gray, s5). The significant inter-brain coherences (top) are color-coded according to the segments in which they are significant (see also Tognoli et al., 2011a).

Figure 4

Correlation between wavelet powers in medial centro-parietal electrodes of leader and follower in instances of dyadic wavelet power patterns specific to (A) low and (B) high leader readiness, respectively. f/Hz stands for frequencies in Hz. The different roles in this segment are the follower acting as signaler and the leader acting as receiver.