<p>Understanding how group-level dynamics arise from individual interactions remains a core challenge in collective behavior research. Traditional models assume animals follow simple behavioral rules, like explicitly aligning with neighbors. We present here an alternative theoretical framework that considers collective behavior to be grounded in neurobiological principles—particularly that animals employ ring attractor networks to encode bearings towards objects in space in an allocentric (i.e., with respect to a fixed external reference frame, such as a stable landmark) and/or egocentric (i.e., the angle relative to the animal’s heading) neural coding. We find collective motion can emerge spontaneously when individuals act as sensory inputs to each other’s networks, but only if individuals employ allocentric bearings to neighbors. Rapid switching between both representations can, however, enhance coordination. Collective motion can, therefore, emerge directly from navigational circuits, and thus may readily evolve, without requiring explicit alignment, or additional rules of interaction.</p>