Linking signal detection theory and encoding models to reveal independent neural representations from neuroimaging data

Many research questions in visual perception involve determining whether stimulus properties are represented and processed independently. In visual neuroscience, there is great interest in determining whether important object dimensions are represented independently in the brain. For example, theories of face recognition have proposed either completely or partially independent processing of identity and emotional expression. Unfortunately, most previous research has only vaguely defined what is meant by “independence,” which hinders its precise quantification and testing. This article develops a new quantitative framework that links signal detection theory from psychophysics and encoding models from computational neuroscience, focusing on a special form of independence defined in the psychophysics literature: perceptual separability. The new theory allowed us, for the first time, to precisely define separability of neural representations and to theoretically link behavioral and brain measures of separability. The framework formally specifies the relation between these different levels of perceptual and brain representation, providing the tools for a truly integrative research approach. In particular, the theory identifies exactly what valid inferences can be made about independent encoding of stimulus dimensions from the results of multivariate analyses of neuroimaging data and psychophysical studies. In addition, commonly used operational tests of independence are re-interpreted within this new theoretical framework, providing insights on their correct use and interpretation. Finally, we apply this new framework to the study of separability of brain representations of face identity and emotional expression (neutral/sad) in a human fMRI study with male and female participants.Author summary: A common question in vision research is whether certain stimulus properties, like face identity and expression, are represented and processed independently. We develop a theoretical framework that allowed us, for the first time, to link behavioral and brain measures of independence. Unlike previous approaches, our framework formally specifies the relation between these different levels of perceptual and brain representation, providing the tools for a truly integrative research approach in the study of independence. This allows to identify what kind of inferences can be made about brain representations from multivariate analyses of neuroimaging data or psychophysical studies. We apply this framework to the study of independent processing of face identity and expression.