Phase maintenance in a rhythmic motor pattern during temperature changes in vivo

Abstract

Central-pattern-generating neural circuits function reliably throughout an animal's life, despite constant molecular turnover and environmental perturbations. Fluctuations in temperature pose a problem to the nervous systems of poikilotherms because their body temperature follows the ambient temperature, thus affecting the temperature-dependent dynamics of various subcellular components that constitute neuronal circuits. In the crustacean stomatogastric nervous system, the pyloric circuit produces a triphasic rhythm comprising the output of the pyloric dilator, lateral pyloric, and pyloric constrictor neurons. In vitro, the phase relationships of these neurons are maintained over a fourfold change in pyloric frequency as temperature increases from 7°C to 23°C. To determine whether these temperature effects are also found in intact crabs, in the presence of sensory feedback and neuromodulator-rich environments, we measured the temperature dependence of the pyloric frequency and phases in vivo by implanting extracellular electrodes into Cancer borealis and Cancer pagurus and shifting tank water temperature from 11°C to 26°C. Pyloric frequency in the intact crab increased significantly with temperature (Q10 = 2-2.5), while pyloric phases were generally conserved. For a subset of the C. borealis experiments, animals were subsequently dissected and the stomatogastric ganglion subjected to a similar temperature ramp in vitro. We found that the maximal frequency attained at high temperatures in vivo is lower than it is under in vitro conditions. Our results demonstrate that, over a wide temperature range, the phases of the pyloric rhythm in vivo are generally preserved, but that the frequency range is more restricted than it is in vitro.

Sources and range of long-term variability of rhythmic motor patternsin vivo.

“…In contrast, the structure of the rhythm, as assessed by the phasing of the pyloric neurons, tends to be much more stable in response to environmental variations (Soofi et al, 2014). We tested whether the structure of the pyloric motoneurons remained stable over long periods of time and during phases when the cycle frequency of the pyloric rhythm changed considerably (Fig.…”

“…We characterized the structure of the pyloric rhythm using aspects of LP activity over long periods of time. We restricted our analysis to the LP neuron, because this neuron has been shown to be the most sensitive to perturbations (Tang et al, 2012;Marder et al, 2014;Soofi et al, 2014). Fig.…”

“…We performed long-term in vivo motor pattern recordings from the lateral ventricular nerve (lvn; similar to Soofi et al, 2014) in the crab Cancer borealis Stimpson 1859. We anesthetized the crab on ice for 30-50 min, cut open the dorsal side of the carapace and located the lvn (Fig.…”

“…In particular, the range of variation in cycle frequency and phase relationships, as well as the range in response to various external and internal influences that these rhythms display is mostly unclear (Heinzel et al, 1993;Hedrich et al, 2011;Diehl et al, 2013;Soofi et al, 2014). For example, the in vivo activity patterns described so far for the pyloric rhythm (Soofi et al, 2014;Clemens et al, 1998a,b) reflect the canonical pyloric pattern, but show no signs of the expected plasticity inferred from neuromodulation experiments in the isolated system. This is surprising because in general, animals are continuously exposed to both predictable (e.g.…”

“…This phase relationship of the pyloric neurons is exceptionally well maintained in vitro, within and between animals , as well as between species (Stein and Städele, 2016). Phase constancy is even maintained when the system is perturbed with varying temperatures (Marder et al, 2015;Soofi et al, 2014), despite a dramatic change in pyloric cycle frequency.…”