No Free Lunch from Deep Learning in Neuroscience: A Case Study through Models of the Entorhinal-Hippocampal Circuit

Abstract Research in Neuroscience, as in many scientific disciplines, is undergoing a renaissance based on deep learning. Unique to Neuroscience, deep learning models can be used not only as a tool but interpreted as models of the brain. The central claims of recent deep learning-based models of brain circuits are that they make novel predictions about neural phenomena or shed light on the fundamental functions being optimized. We show, through the case-study of grid cells in the entorhinal-hippocampal circuit, that one may get neither. We begin by reviewing the principles of grid cell mechanism and function obtained from first-principles modeling efforts, then rigorously examine the claims of deep learning models of grid cells. Using large-scale architectural and hyperparameter sweeps and theory-driven experimentation, we demonstrate that the results of such models may be more strongly driven by particular, non-fundamental, and post-hoc implementation choices than fundamental truths about neural circuits or the loss function(s) they might optimize. We discuss why these models cannot be expected to produce accurate models of the brain without the addition of substantial amounts of inductive bias, an informal No Free Lunch result for Neuroscience. Based on first principles work, we provide hypotheses for what additional loss functions will produce grid cells more robustly. In conclusion, circumspection and transparency, together with biological knowledge, are warranted in building and interpreting deep learning models in Neuroscience.