From the intrinsic properties to the functional role of a neuron phenotype: an example from electric fish during signal trade-off

Abstract

SummaryThis review deals with the question: what is the relationship between the properties of a neuron and the role that the neuron plays within a given neural circuit? Answering this kind of question requires collecting evidence from multiple neuron phenotypes and comparing the role of each type in circuits that perform well-defined computational tasks. The focus here is on the spherical neurons in the electrosensory lobe of the electric fish Gymnotus omarorum. They belong to the one-spike-onset phenotype expressed at the early stages of signal processing in various sensory modalities and diverse taxa. First, we refer to the one-spike neuron intrinsic properties, their foundation on a low-threshold K + conductance, and the potential roles of this phenotype in different circuits within a comparative framework. Second, we present a brief description of the active electric sense of weakly electric fish and the particularities of spherical one-spike-onset neurons in the electrosensory lobe of G. omarorum. Third, we introduce one of the specific tasks in which these neurons are involved: the trade-off between self-and allo-generated signals. Fourth, we discuss recent evidence indicating a still-undescribed role for the one-spike phenotype. This role deals with the blockage of the pathway after being activated by the self-generated electric organ discharge and how this blockage favors selfgenerated electrosensory information in the context of allo-generated interference. Based on comparative analysis we conclude that one-spike-onset neurons may play several functional roles in animal sensory behavior. There are specific adaptations of the neuronʼs ʻresponse functionʼ to the circuit and task. Conversely, the way in which a task is accomplished depends on the intrinsic properties of the neurons involved. In short, the role of a neuron within a circuit depends on the neuron and its functional context.

A fast BK-type KCa current acts as a postsynaptic modulator of temporal selectivity for communication signals

“…In the electrosensory system of wave-type electric fishes, Ca 2+ -dependent (Ellis et al, 2007; Krahe et al, 2008; Mehaffey et al, 2008) and voltage-dependent conductances (Fortune and Rose, 1997, 2003; Carlson and Kawasaki, 2006; Nogueira and Caputi, 2013) are also suggested to regulate frequency and AM-frequency tuning. To our knowledge, this study is the first to directly examine the intrinsic membrane properties that underlie selectivity for interspike intervals.…”

The bioinspiring potential of weakly electric fish

“…The presence of various types of electroreceptors heterogeneously distributed, imply that the physical electric image can be encoded at the early stages as a set of different neural images which represent the outer space with different resolution. This is expressed as a set of somatotopically arranged maps in which a deformed shape of the fish Second, electroreceptors tuned to the EOD can be classified in general in two broad types, those that respond to the stimulus with a single spike 9 at a nearly fixed latency (giving origin to the so called fast electrosensory pathways, [61,114,150]) and those that respond with trains of spikes modulated by the characteristics of the stimulus (giving origin to the so called slow electrosensory pathway [150]). Depending on the species electroreceptors are able to sense or not frequency spectral changes which give them the possibility to process images in some kind of 'electric color' [34,108,155].…”

Waveform discrimination in a pair of pulse‐generating electric fishes

“…This timing was selected because it avoids interference with the subsequent EOD, as well as early processing of self‐generated signals. This delay mimics the natural behaviour of synchronization bouts observed in these species (Westby, ) and also avoids temporal overlap of the stimulus with (a) the EOD and the time window necessary for early processing of self‐generated signals (Nogueira & Caputi, , ; Pereira et al ., ) and (b) the time windows triggering the jamming avoidance responses (Bullock, ; Capurro et al ., ; Nogueira & Caputi, , ; Westby, ). To ensure that playback signals had the same strength and were in the range of both species in natural conditions, they were generated at a value intermediate to those found in the initial recordings (RMS = 1226 μV cm –1 ).…”