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 non-responsive to moving stimuli. Remarkably, we found that non-responsive 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. Further, addition of non-responsive neurons in the model gave rise to synergistic population coding. Taken together, our findings reveal that non-responsive 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 non-responsive neurons have been observed in sensory systems across taxa; it is likely that similar synergistic interactions improve population coding across modalities and behavioral tasks.Significance Statement Here we show that including the activities of non-responsive neurons with those of responsive neurons increases Fisher information about stimulus location. Further analysis revealed that this is because including non-responsive neurons led to reduced noise levels for responsive neurons. A combination of multi-unit recordings from neural populations and mathematical modeling reveals that response heterogeneity and spatially decaying correlations are necessary to observe this effect. It is likely that synergistic population coding by responsive and non-responsive neurons will be observed in other systems.
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