Abstract
Heterogeneity of neural properties within a given neural class is ubiquitous in the nervous system and permits different sub-classes of neurons to specialize for specific purposes. This principle has been thoroughly investigated in the hindbrain of the weakly electric fish A. leptorhynchus in the primary electrosensory area, the Electrosensory Lateral Line lobe (ELL). The pyramidal cells (PCs) that receive inputs from tuberous electroreceptors are organized in three maps in distinct segments of the ELL. The properties of these cells vary greatly across maps due to differences in connectivity, receptor expression, and ion channel composition. These cells are a seminal example of bursting neurons and their bursting dynamic relies on the presence of voltage-gated Na+ channels in the extensive apical dendrites of the superficial PCs. Other ion channels can affect burst generation and their expression varies across ELL neurons and segments. For example, SK channels cause hyperpolarizing after-potentials decreasing the likelihood of bursting, yet bursting propensity is similar across segments. We question whether the depolarizing mechanism that generates the bursts presents quantitative differences across segments that could counterbalance other differences having the opposite effect. Although their presence and role are established, the distribution and density of the apical dendrites’ Na+ channels have not been quantified and compared across ELL maps. Therefore, we test the hypothesis that Na+ channel density varies across segment by quantifying their distribution in the apical dendrites of immunolabeled ELL sections. We found the Na+ channels to be two-fold denser in the lateral segment (LS) than in the centro-medial segment (CMS), the centro-lateral segment (CLS) being intermediate. Our results imply that this differential expression of voltage-gated Na+ channels could counterbalance or interact with other aspects of neuronal physiology that vary across segments (e.g., SK channels). We argue that burst coding of sensory signals, and the way the network regulates bursting, should be influenced by these variations in Na+ channel density.
Highlights
Neurons possess a variety of ion channels and membrane proteins that shape their response properties, from the classical Na+ and K+ ion channels generating action potentials to G-protein coupled receptors (e.g., Prešern et al, 2015; Duménieu et al, 2017; Lizbinski et al, 2018)
Prior to visualizing the Nav labeling, we selected in each scan 2–4 portions of dendrites that are clearly delineated by the MAP2 labeling
The principal finding of the present experiment was that lateral segment (LS) exhibits the highest dendritic Nav channel density, followed by centro-lateral segment (CLS) and centro-medial segment (CMS)
Summary
Neurons possess a variety of ion channels and membrane proteins that shape their response properties, from the classical Na+ and K+ ion channels generating action potentials to G-protein coupled receptors (e.g., Prešern et al, 2015; Duménieu et al, 2017; Lizbinski et al, 2018). The complementary, but non-exclusive, principle is a basic concept in neuroscience This principle argues that changes in membrane proteins (e.g., voltage gated ions channels) are necessary for specialization of neurons, and result in different neural outputs (Hille, 2001). An example of this principle, central to the subject of our study, comes from neurons that possess specific ionic conductances responsible for generating burst firing (Krahe and Gabbiani, 2004). The neuron’s bursting dynamic could not be possible without these specific ion channels and their role in neural coding is changed by this bursting dynamic
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