Animals are capable of navigation even in the absence of prominent landmark cues. This behavioral demonstration of path integration is supported by the discovery of place cells and other neurons that show path-invariant response properties even in the dark. That is, under suitable conditions, the activity of these neurons depends primarily on the spatial location of the animal regardless of which trajectory it followed to reach that position. Although many models of path integration have been proposed, no known single theoretical framework can formally accommodate their diverse computational mechanisms. Here we derive a set of necessary and sufficient conditions for a general class of systems that performs exact path integration. These conditions include multiplicative modulation by velocity inputs and a path-invariance condition that limits the structure of connections in the underlying neural network. In particular, for a linear system to satisfy the pathinvariance condition, the effective synaptic weight matrices under different velocities must commute. Our theory subsumes several existing exact path integration models as special cases. We use entorhinal grid cells as an example to demonstrate that our framework can provide useful guidance for finding unexpected solutions to the path integration problem. This framework may help constrain future experimental and modeling studies pertaining to a broad class of neural integration systems.commutativity | attractor network | oscillatory interference | dead reckoning | Fourier analysis E ven without allothetic or environmental cues, animals are capable of finding their way home (1, 2), a process known as path integration or dead reckoning. This "integrative process" (3), whereby an internal representation of position is updated by incoming inertial or self-motion cues, was hypothesized over a century ago by Darwin (4) and Murphy (3). More recently, potential neural correlates of path integration have been discovered. For example, cells in brain regions associated with the Papez circuit can signal the heading direction of an animal (5, 6); grid cells in the entorhinal cortex presumably integrate this information and other self-motion cues to form a periodic spatial code (7-9); and, downstream in the hippocampus, place cells exhibit a sparser location code (10, 11).Many computational models of path integration have been proposed. For instance, two leading classes of models of grid cells are continuous attractor networks (12-14) and oscillatory interference models (15)(16)(17)(18)(19)(20). These diverse models seemingly describe a diverse class of systems; however, deeper computational principles may exist that unify the different cases of neural integration. Here we attempt to identify a general principle of path integration by starting with the exact requirement of invariance to movement trajectory in an arbitrary number of dimensions. This general approach allows us to derive a set of necessary and sufficient conditions for path integration and, for linear systems,...