Circuit Robustness to Temperature Perturbation Is Altered by Neuromodulators

Abstract

SUMMARY In the ocean, the crab, Cancer borealis, is subject to daily and seasonal temperature changes. Previous work, done in the presence of descending modulatory inputs, had shown that the pyloric rhythm of the crab increases in frequency as temperature increases, but maintains its characteristic phase relationships until it “crashes” at extreme high temperatures. To study the interaction between neuromodulators and temperature perturbations, we studied the effects of temperature on preparations from which the descending modulatory inputs were removed. Under these conditions the pyloric rhythm was destabilized. We then studied the effects of temperature on preparations in the presence of oxotremorine, proctolin, and serotonin. Oxotremorine and proctolin enhanced the robustness of the pyloric rhythm, while serotonin made the rhythm less robust. These experiments reveal considerable animal-to-animal diversity in their crash stability, consistent with the interpretation that cryptic differences in many cell and network parameters are revealed by extreme perturbations.

Temperature compensation in a small rhythmic circuit

“…In this work, we build on the results in Caplan et al, 2014 and implemented temperature sensitivity in a model of the pyloric network ( Prinz et al, 2004 ). We show that in these models, there are multiple sets of maximal conductances and temperature sensitivities that reproduce much of the experimental phenomenology previously reported ( Tang et al, 2010 ; Tang et al, 2012 ; Soofi et al, 2014 ; Haddad and Marder, 2018 ). In addition, we explored how the dynamics of the currents are modified to sustain the correct activity at each temperature.…”

“…Because the contribution of a given current to a neuronal process can be replaced by another at different temperatures, deletion or blockade of a current can produce qualitatively different effects at high and low temperatures. These results provide a plausible hypothesis for why interactions between temperature and a second perturbation can be observed experimentally ( Haddad and Marder, 2018 ; Ratliff et al, 2018 ).…”

“…For temperatures higher than a critical temperature, the biological network displays anomalous regimes characterized by the emergence of slow time scales and intermittency between what appear to be metastable states ( Tang et al, 2012 ; Haddad and Marder, 2018 ). At temperatures higher than 25°C some models do not display irregular behavior but just become quiescent, or produce subthreshold oscillations.…”

“…This behavior is robust and stable, and the cells and their connections are well-characterized. Robustness to temperature in the pyloric network has been explored experimentally by Tang et al, 2010 ; Tang et al, 2012 ; Soofi et al, 2014 and Haddad and Marder, 2018 . These studies show that as temperature increases the frequency of the pyloric rhythm increases but the phases of the cycle at which each cell is active remain approximately constant.…”

On the interpretation of results obtained in singly housed animals

“…The concept has been nicely illustrated by Eve Marder's group . They showed that different animals respond differently to the same external challenge . The biological disparities between animals constrain the form of the response.…”