Fast burst fraction transients convey information independent of the firing rate

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Abstract

Theories of attention and learning have hypothesized a central role for high-frequency bursting in cognitive functions, but experimental reports of burst-mediated representations \emph{in vivo} have been limited. Here we used a novel demultiplexing approach by considering a conjunctive burst code. We studied this code \emph{in vivo} while animals learned to report direct electrical stimulation of the somatosensory cortex and found two acquired yet independent representations. One code, the event rate, showed a sparse and succint stiumulus representation and a small modulation upon detection errors. The other code, the burst fraction, correlated more globally with stimulation and more promptly responded to detection errors. Potent and fast modulations of the burst fraction were seen 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 the firing rate response, and was strongly associated with behavioral accuracy. Thus a fine-grained 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 implement attention mechanisms.

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