Scale-free dynamics in animal groups and brain networks

Abstract

Collective phenomena fascinate by the emergence of order in systems composed of a myriad of small entities. They are ubiquitous in nature and can be found over a vast range of scales in physical and biological systems. Their key feature is the seemingly effortless emergence of adaptive collective behavior that cannot be trivially explained by the properties of the system’s individual components. This perspective focuses on recent insights into the similarities of correlations for two apparently disparate phenomena: flocking in animal groups and neuronal ensemble activity in the brain. We first will summarize findings on the spontaneous organization in bird flocks and macro-scale human brain activity utilizing correlation functions and insights from critical dynamics. We then will discuss recent experimental findings that apply these approaches to the collective response of neurons to visual and motor processing, i.e. to local perturbations of neuronal networks at the meso- and microscale. We show how scale-free correlation functions capture the collective organization of neuronal avalanches in evoked neuronal populations in nonhuman primates and between neurons during visual processing in rodents. These experimental findings suggest that the coherent collective neural activity observed at scales much larger than the length of the direct neuronal interactions is demonstrative of a phase transition. We discuss the experimental support for either discontinuous or continuous phase transitions. We conclude that at or near a phase-transition neuronal information can propagate in the brain with the same efficiency as proposed to occur in the collective adaptive response observed in some animal groups.

Using neuronal models to capture burst-and-glide motion and leadership in fish

“…Less direct analogies have previously been made between collective motion and activities in the brain. For example, Marshall et al draw parallels between decision-making in ants and decision-making in primate brains [ 52 ], Passino et al show that some main characteristics of cognition in brains of vertebrates are also present in swarms of honey bees [ 53 ], and on a more general level, Ribeiro et al discuss the connections between animal group dynamics and networks in brains [ 54 ]. There are also existing models connecting sensory systems to neuronal dynamics.…”

Subcritical escape waves in schooling fish

“…For animal collectives, signatures of near criticality have been observed in bird flocks (17), mammals (7), insects (18,19), and fish schools (20), while theoretical models have investigated maximal sensitivity at the critical regime (21)(22)(23)(24). Predominantly, these studies considered the system's maximal sensitivity or flexibility or the appearance of long-ranged correlations within it as possible benefits of criticality to animals within collectives (25). However, while individuals within animal groups can benefit from social information provided by others (26), environmental and internal noise may also result in individuals making erroneous decisions, resulting in them providing misleading social cues (27,28).…”