Receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays.

Abstract

Studies on population coding implicitly assume that spikes from the presynaptic population arrive simultaneously at the integrating neuron. In natural neuronal populations, this is usually not the case -- neuronal signalling takes time and neuronal populations cover a certain space. The spread of spike arrival times depends on population size, cell density and axonal conduction velocity. We here analyze the consequences of population size and axonal conduction delays on the stimulus encoding performance in the electrosensory system of the electric fish Apteronotus leptorhynchus. We experimentally locate p-type electroreceptor afferents along the rostro-caudal body axis and relate locations to neurophysiological response properties. In an information-theoretical approach we analyze the coding performance in homogeneous and heterogeneous populations. As expected, the amount of information increases with population size and, on average, heterogeneous populations encode better than the average same-size homogeneous population if conduction delays are compensated for. The spread of neuronal conduction delays within a receptive field strongly degrades encoding of high-frequency stimulus components. Receptive field sizes typically found in the electrosensory lateral line lobe of A. leptorhynchus appear to be a good compromise between the spread of conduction delays and encoding performance. The limitations imposed by finite axonal conduction velocity are relevant for any converging network as is shown by model populations of LIF neurons. The bandwidth of natural stimuli and the maximum meaningful population sizes are constrained by conduction delays and may thus impact the optimal design of nervous systems. Author summaryReading out the activity of a population of neurons can yield a more complete picture of the stimulus space. Generally, increasing population sizes increases the amount of information. This applies to homogeneous populations of similarly tuned neurons as well as heterogeneous populations. So far studies on population coding assumed the information to reach the integrating neuron simultanously. But neurons are neither disembodied nor does neuronal signalling happen instantaneously; populations cover a certain space and axonal conduction takes time. The interplay of encoding bandwidth, receptive field respectively population size and axonal conduction velocity has not been addressed before. Our results from the electrosensory system and of model simulations show that stimulus dynamics, receptive field sizes, and conduction velocity have to be factored in when we want to understand the design of nervous systems.