Understanding collective behavior through neurobiology

Abstract

A variety of organisms exhibit collective movement, including schooling fish and flocking birds, where coordinated behavior emerges from the interactions between group members. Despite the prevalence of collective movement in nature, little is known about the neural mechanisms producing each individual's behavior within the group. Here we discuss how a neurobiological approach can enrich our understanding of collective behavior by determining the mechanisms by which individuals interact. We provide examples of sensory systems for social communication during collective movement, highlight recent discoveries about neural systems for detecting the position and actions of social partners, and discuss opportunities for future research. Understanding the neurobiology of collective behavior can provide insight into how nervous systems function in a dynamic social world.

Figure 1. Diversity of sensory systems underlying collective behavior.

Displayed are examples of the diverse set of sensory systems underlying collective behavior in various species, where individuals sense the position and actions of others to produce cooperative movement. Schematics of sensations and primary sensory organs are depicted in orange and green, respectively. Vision: eye and retinal ganglion cells in the retina of schooling fish and flocking birds. Mechanosensation: hair cells in Drosophila leg bristles and in neuromasts of fish lateral line. Chemosensation: olfactory receptor neurons in ants. Audition: hair cells in the cochlea of bats and dolphins. Electrosensation: electroreceptors in the ampullary and tuberous organs of the electric fish and skates.

Figure 2. Neural circuits in individuals that support emergent collective behavior.

Displayed is a schematic of our current neurobiological understanding of how an individual animal perceives its social partners in its environment. On the left is a school of fish coordinating their movements with one another. Although all members of the school are actively observing the others, we focus on one focal fish to illustrate this process - with its visual fields depicted in orange. On the right is a broad schematic of the hypothesized sensory-motor transformation that occurs within the fish brain during collective movement, including the unknown central computations that link sensory detection to motor translation. At the top is the primary visual system of the fish (orange) – the retinal neural layers that transduce visual information. In the center are hypothesized neural circuits, whose structure and dynamics are unknown. On the bottom is the premotor system of the fish (purple), with a focus on brainstem spinal projection neurons that control movement - in this case the alignment, repulsion, and/or attraction to the other fish. Multiple stages of this network are likely influenced by a number of other factors, including but not limited to each of the items denoted in blue on the right.