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The backpropagation of error algorithm (backprop) has been instrumental in the recent success of deep learning. However, a key question remains as to whether backprop can be formulated in a manner suitable for implementation in neural circuitry. The primary challenge is to ensure that any candidate formulation uses only local information, rather than relying on global signals as in standard backprop. Recently several algorithms for approximating backprop using only local signals have been proposed. However, these algorithms typically impose other requirements which challenge biological plausibility: for example, requiring complex and precise connectivity schemes, or multiple sequential backwards phases with information being stored across phases. Here, we propose a novel algorithm, Activation Relaxation (AR), which is motivated by constructing the backpropagation gradient as the equilibrium point of a dynamical system. Our algorithm converges rapidly and robustly to the correct backpropagation gradients, requires only a single type of computational unit, utilises only a single parallel backwards relaxation phase, and can operate on arbitrary computation graphs. We illustrate these properties by training deep neural networks on visual classification tasks, and describe simplifications to the algorithm which remove further obstacles to neurobiological implementation (for example, the weight-transport problem, and the use of nonlinear derivatives), while preserving performance.