Information transmission by multiple pyramidal cells in the hindbrain of weakly electric fish

Ruediger Krahe, Gabriel Kreiman, Fabrizio Gabbiani, Christof Koch, and Walter Metzner

Annual Meeting of the Society for Neuroscience, San Diego, 2001

Are highly correlated responses of nearby neurons within topographic sensory maps merely a sign of redundant information transmission or do they carry relevant information? To tackle this problem we recorded simultaneously from pairs of electrosensory pyramidal cells (PCs) in a somatotopic map in the electrosensory lateral line lobe of the weakly electric fish, Eigenmannia, while randomly modulating the amplitude of a mimic of the animal's electric field. Previous work had shown that single PCs encode the stimulus time course only poorly. Instead, they extract upstrokes and downstrokes in stimulus amplitude by firing short bursts of spikes which reliably indicate the presence of behaviorally relevant stimulus features. Extending these approaches to pairs of PCs with overlapping receptive fields, we found that: (1) PC-pairs exhibit strong correlations on a time scale of several tens of milliseconds, mainly due to time-locking of spikes to the stimulus and not to common synaptic input. (2) This was corroborated by Neurobiotin-labeling of primary afferent fibers, yielding an estimated divergence of one afferent fiber onto only 3-8 PCs. (3) In a feature-extraction task, PC-pairs perform significantly better than single PCs. Thus, our results demonstrate that while the occurrence of stimulus features can be reliably indicated by spike bursts of single PCs, this reliability significantly increases by considering stimulus-induced coincident activity across multiple neurons, i.e. by evaluating "distributed bursts" of spikes. Supported by NSF