Nonlinear Hebbian Learning as a Unifying Principle in Receptive Field Formation

The development of sensory receptive fields has been modeled in the past by a variety of models including normative models such as sparse coding or independent component analysis and bottom-up models such as spike-timing dependent plasticity or the Bienenstock-Cooper-Munro model of synaptic plasticity. Here we show that the above variety of approaches can all be unified into a single common principle, namely nonlinear Hebbian learning. When nonlinear Hebbian learning is applied to natural images, receptive field shapes were strongly constrained by the input statistics and preprocessing, but exhibited only modest variation across different choices of nonlinearities in neuron models or synaptic plasticity rules. Neither overcompleteness nor sparse network activity are necessary for the development of localized receptive fields. The analysis of alternative sensory modalities such as auditory models or V2 development lead to the same conclusions. In all examples, receptive fields can be predicted a priori by reformulating an abstract model as nonlinear Hebbian learning. Thus nonlinear Hebbian learning and natural statistics can account for many aspects of receptive field formation across models and sensory modalities.Author Summary: The question of how the brain self-organizes to develop precisely tuned neurons has puzzled neuroscientists at least since the discoveries of Hubel and Wiesel. In the past decades, a variety of theories and models have been proposed to describe receptive field formation, notably V1 simple cells, from natural inputs. We cut through the jungle of candidate explanations by demonstrating that in fact a single principle is sufficient to explain receptive field development. Our results follow from two major insights. First, we show that many representative models of sensory development are in fact implementing variations of a common principle: nonlinear Hebbian learning. Second, we reveal that nonlinear Hebbian learning is sufficient for receptive field formation through sensory inputs. The surprising result is that our findings are robust of specific details of a model, and allows for robust predictions on the learned receptive fields. Nonlinear Hebbian learning is therefore general in two senses: it applies to many models developed by theoreticians, and to many sensory modalities studied by experimental neuroscientists.