Postsynaptic Receptive Field Size and Spike Threshold Determine Encoding of High-frequency Information via Sensitivity to Synchronous Presynaptic Activity

Parallel sensory streams carrying distinct information about various stimulus properties have been observed in several sensory systems, including the visual system. What remains unclear is why some of these streams differ in the size of their receptive fields (RFs). In the electrosensory system, neurons with large RFs have short-latency responses and are tuned to high-frequency inputs. Conversely, neurons with small RFs are low-frequency tuned and exhibit longer-latency responses. What principle underlies this organization? We show experimentally that synchronous electroreceptor afferent (P-unit) spike trains selectively encode high-frequency stimulus information from broadband signals. This finding relies on a comparison of stimulus-spike output coherence using output trains obtained by either summing pairs of recorded afferent spike trains or selecting synchronous spike trains based on coincidence within a small time window. We propose a physiologically realistic decoding mechanism, based on postsynaptic RF size and postsynaptic output rate normalization that tunes target pyramidal cells in different electrosensory maps to low- or high-frequency signal components. By driving realistic neuron models with experimentally obtained P-unit spike trains, we show that a small RF is matched with a postsynaptic integration regime leading to responses over a broad range of frequencies, and a large RF with a fluctuation-driven regime that requires synchronous presynaptic input and therefore selectively encodes higher frequencies, confirming recent experimental data. Thus our work reveals that the frequency content of a broadband stimulus extracted by pyramidal cells, from P-unit afferents, depends on the amount of feedforward convergence they receive.