Model-brain comparison using inter-animal transforms

Abstract

Artificial neural network models have emerged as promising mechanistic models of the brain. However, there is little consensus on the correct method for comparing model activations to brain responses. Drawing on recent work in philosophy of neuroscience, we propose a comparison methodology based on the Inter-Animal Transform Class (IATC) - the strictest set of functions needed to accurately map neural responses between subjects in an animal population. Using the IATC, we can map bidirectionally between a candidate model's responses and brain data, assessing how well the model can masquerade as a typical subject using the same kinds of transforms needed to map across real subjects. We identify the IATC in three settings: a simulated population of neural network models, a population of mouse subjects, and a population of human subjects. We find that the IATC resolves detailed aspects of the neural mechanism, such as the non-linear activation function. Most importantly, we find that the IATC enables accurate predictions of neural activity while also achieving high specificity in mechanism identification, evidenced by its ability to separate response patterns from different brain areas while strongly aligning same-brain-area responses between subjects. In other words, the IATC is a proof-by-existence that there is no inherent tradeoff between the neural engineering goal of high model-brain predictivity and the neuroscientific goal of identifying mechanistically accurate brain models. Using IATC-guided transforms, we obtain new evidence in favor of topographical deep neural networks (TDANNs) as models of the visual system. Overall, the IATC enables principled model-brain comparisons, contextualizing previous findings about the predictive success of deep learning models of the brain, while improving upon previous approaches to model-brain comparison.