Co-variation of ionic conductances supports phase maintenance in stomatogastric neurons

Abstract

Neuronal networks produce reliable functional output throughout the lifespan of an animal despite ceaseless molecular turnover and a constantly changing environment. Central pattern generators, such as those of the crustacean stomatogastric ganglion (STG), are able to robustly maintain their functionality over a wide range of burst periods. Previous experimental work involving extracellular recordings of the pyloric pattern of the STG has demonstrated that as the burst period varies, the inter-neuronal delays are altered proportionally, resulting in burst phases that are roughly invariant. The question whether spike delays within bursts are also proportional to pyloric period has not been explored in detail. The mechanism by which the pyloric neurons accomplish phase maintenance is currently not obvious. Previous studies suggest that the co-regulation of certain ion channel properties may play a role in governing neuronal activity. Here, we observed in long-term recordings of the pyloric rhythm that spike delays can vary proportionally with burst period, so that spike phase is maintained. We then used a conductance-based model neuron to determine whether co-varying ionic membrane conductances results in neural output that emulates the experimentally observed phenomenon of spike phase maintenance. Next, we utilized a model neuron database to determine whether conductance correlations exist in model neuron populations with highly maintained spike phases. We found that co-varying certain conductances, including the sodium and transient calcium conductance pair, causes the model neuron to maintain a specific spike phase pattern. Results indicate a possible relationship between conductance co-regulation and phase maintenance in STG neurons.

Differential effects of conductances on the phase resetting curve of a bursting neuronal oscillator

“…Another interesting avenue of exploration is whether certain pairs of conductances result in the preservation of PRC shape. Several studies have demonstrated that parameters at the mRNA (Schulz et al 2007; Tobin et al 2009), cellular (Soofi et al 2012; Ball et al 2010; Hudson and Prinz 2010), and synaptic (Goaillard et al 2009) levels exhibit pairwise correlations within solution spaces. Examining whether pairwise correlations also preserve PRC shape is a natural extension of these studies, since the PRC provides a functional view of the neuron’s role in determining network-level output.…”

The Integrative Role of the Sigh in Psychology, Physiology, Pathology, and Neurobiology

“…5B). However, the complement of these currents varies, and every individual neuron establishes a different dynamic balance of inward and outward currents, a principle that has been well documented for invertebrate neurons (Hudson and Prinz, 2010; Khorkova and Golowasch, 2007; Soofi et al, 2012; Temporal et al, 2012; Zhao and Golowasch, 2012). As a result, some neurons within the respiratory network are more bursting than others; some burst regularly, some are irregular, some discharge tonically, and some are silent (Carroll and Ramirez, 2013; Garcia et al, 2011; Koch et al, 2011; Ramirez et al, 2011, 2012; Viemari and Ramirez, 2006).…”

Ionic Current Variability and Functional Stability in the Nervous System

“…This question applies equally to cases of individual variability and to those of population variability, although the mechanisms that may generate these two distinct classes of variability could differ. Theoretical work predicts that this should be the case (Burdakov 2005, Olypher and Calabrese 2007, Taylor et al 2009, Ball et al 2010, Hudson and Prinz 2010, Soofi et al 2012, Lamb and Calabrese 2013). Most of these studies show that linear or nearly linear combinations of the maximal conductances of two or more ionic currents (conductance correlations) define regions in parameter space in which activity traits are fixed, although linear relations are not always what is needed.…”