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

• Published in: PLoS computational biology Vol. 19; no. 8; p. e1010871
• Main Authors: Hladnik, Tim C, Grewe, Jan
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.08.2023; Public Library of Science (PLoS)
• Subjects: Anesthesia; Animals; Axons; Bandwidth; Bandwidths; Biology and Life Sciences; Cell density; Cell size; Coding; Electric Fish - physiology; Electric Organ - physiology; Electric organs in fishes; Electrodes; Electrophysiology; Electrosensory system; Engineering and Technology; Lateral line; Neural coding; Neurons; Physiological aspects; Population density; Population number; Population studies; Populations; Receptive field; Research and Analysis Methods; Skin; Social Sciences; Surgery; Synapses; Velocity; Zoological research; Germany; United States > US
• ISSN: 1553-7358; 1553-734X; 1553-7358
• DOI: 10.1371/journal.pcbi.1010871

Studies on population coding implicitly assume that spikes from the presynaptic cells arrive simultaneously at the integrating neuron. In natural neuronal populations, this is usually not the case-neuronal signaling takes time and populations cover a certain space. The spread of spike arrival times depends on population size, cell density and axonal conduction velocity. Here we 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.