Neuronal firing rate diversity lowers the dimension of population covariability

Abstract

Neuronal responses are very diverse, with specific stimuli or behaviors eliciting a range of activity across a neuronal population. These responses also show large and correlated trial-to-trial fluctuations that occupy a low-dimensional region in activity space. We link these two aspects of neuronal response in both feedforward and recurrent circuit models and derive the following relation: the more diverse the firing rates of neurons in a population, the lower the effective dimension of their trial-to-trial covariability. We test our prediction using simultaneously recorded neuronal populations from numerous brain areas in mice, non-human primates, and in the motor cortex of human participants. Finally, we show how diverse neural codes lead to better stimulus discrimination, and that when the brain is in a heightened state of processing responses are more diverse and have lower-dimensional fluctuations. In sum, we present an organizing principle of population response that is widely observed across the nervous system and acts to synergistically improve population representation.