Nonresponsive Neurons Improve Population Coding of Object Location

Understanding how heterogeneous neural populations represent sensory input to give rise to behavior remains a central problem in systems neuroscience. Here we investigated how midbrain neurons within the electrosensory system of Apteronotus leptorhynchus code for object location in space. In vivo simultaneous recordings were achieved via Neuropixels probes, high-density electrode arrays, with the stimulus positioned at different locations relative to the animal. Midbrain neurons exhibited heterogeneous response profiles, with a significant proportion (65%) seemingly nonresponsive to moving stimuli. Remarkably, we found that nonresponsive neurons increased population coding of object location through synergistic interactions with responsive neurons by effectively reducing noise. Mathematical modeling demonstrated that increased response heterogeneity together with the experimentally observed correlations was sufficient to give rise to independent encoding by responsive neurons. Furthermore, the addition of nonresponsive neurons in the model gave rise to synergistic population coding. Taken together, our findings reveal that nonresponsive neurons, which are frequently excluded from analysis, can significantly improve population coding of object location through synergistic interactions with responsive neurons. Combinations of responsive and nonresponsive neurons have been observed in sensory systems across taxa; it is likely that similar synergistic interactions improve population coding across modalities and behavioral tasks.