A ternary neural code resolves error and sharpening signals

Abstract

ABSTRACTTheories of attention and learning have hypothesized a central role for high-frequency bursting in cognitive functions, but experimental reports of burstmediated representations in vivo have been limited. Here we used a novel demultiplexing approach to separate independent streams of information from considering neurons as having three possible states: silent, singlet- and burst-firing. We studied this ternary neural code in vivo while animals learned to behaviorally report direct electrical stimulation of the somatosensory cortex and found two acquired yet independent representations. One code, the event rate, represented the stimulus in a small fraction of cells and showed a small modulation upon detection errors. The other code, the burst fraction, correlated more globally with stimulation and more promptly responded to detection errors. Bursting modulation was potent and its time course evolved, even in cells that were considered unresponsive based on the firing rate. During the later stages of training, this modulation in bursting happened earlier, gradually aligning temporally with the representation in event rate. The alignment of bursting and event rate modulation sharpened firing rate coded representations, and was strongly associated behavioral accuracy. Thus a fine grain separation of spike timing patterns reveals two signals that accompany stimulus representations: an error signal that can be essential to guide learning and a sharpening signal that could enact top-down attention.