Successful navigation is fundamental to the survival of nearly every animal on earth, and achieved by nervous systems of vastly different sizes and characteristics. Yet surprisingly little is known of the detailed neural circuitry from any species which can accurately represent space for navigation. Path integration is one of the oldest and most ubiquitous navigation strategies in the animal kingdom. Despite a plethora of computational models, from equational to neural network form, there is currently no consensus, even in principle, of how this important phenomenon occurs neurally. Recently, all path integration models were examined according to a novel, unifying classification system. Here we combine this theoretical framework with recent insights from directed walk theory, and develop an intuitive yet mathematically rigorous proof that only one class of neural representation of space can tolerate noise during path integration. This result suggests many existing models of path integration are not biologically plausible due to their intolerance to noise. This surprising result imposes significant computational limitations on the neurobiological spatial representation of all successfully navigating animals, irrespective of species. Indeed, noise-tolerance may be an important functional constraint on the evolution of neuroarchitectural plans in the animal kingdom.