The need to make fast decisions under risky and uncertain conditions is a widespread problem in the natural world. While there has been extensive work on how individual organisms dynamically modify their behavior to respond appropriately to changing environmental conditions (and how this is encoded in the brain), we know remarkably little about the corresponding aspects of collective information processing in animal groups. For example, many groups appear to show increased “sensitivity” in the presence of perceived threat, as evidenced by the increased frequency and magnitude of repeated cascading waves of behavioral change often observed in fish schools and bird flocks under such circumstances. How such context-dependent changes in collective sensitivity are mediated, however, is unknown. Here we address this question using schooling fish as a model system, focusing on 2 nonexclusive hypotheses: 1) that changes in collective responsiveness result from changes in how individuals respond to social cues (i.e., changes to the properties of the “nodes” in the social network), and 2) that they result from changes made to the structural connectivity of the network itself (i.e., the computation is encoded in the “edges” of the network). We find that despite the fact that perceived risk increases the probability for individuals to initiate an alarm, the context-dependent change in collective sensitivity predominantly results not from changes in how individuals respond to social cues, but instead from how individuals modify the spatial structure, and correspondingly the topology of the network of interactions, within the group. Risk is thus encoded as a collective property, emphasizing that in group-living species individual fitness can depend strongly on coupling between scales of behavioral organization.

We study the interplay between network topology and complex space-time patterns and introduce a concept to analytically predict complex patterns in networks of Stuart-Landau oscillators with linear symmetric and instantaneous coupling based solely on the network topology. These patterns consist of partial amplitude death and partial synchronization and are found to exist in large variety for all undirected networks of up to 5 nodes. The underlying concept is proved to be robust with respect to frequency mismatch and can also be extended to larger networks. In addition it directly links the stability of complete in-phase synchronization to only a small subset of topological eigenvalues of a network.

Theoretical physics predicts optimal information processing in living systems near transitions (or pseudo-critical points) in their collective dynamics. However, focusing on potential benefits of proximity to a critical point, such as maximal sensitivity to perturbations and fast dissemination of information, commonly disregards possible costs of criticality in the noisy, dynamic environmental contexts of biological systems. Here, we find that startle cascades in fish schools are subcritical (not maximally responsive to environmental cues) and that distance to criticality decreases when perceived risk increases. Considering individuals’ costs related to two detection error types, associated to both true and false alarms, we argue that being subcritical, and modulating distance to criticality, can be understood as managing a trade-off between sensitivity and robustness according to the riskiness and noisiness of the environment. Our work emphasizes the need for an individual-based and context-dependent perspective on criticality and collective information processing and motivates future questions about the evolutionary forces that brought about a particular trade-off.