Journal Article

The role of feedback and modulation in determining temperature resiliency in the lobster cardiac nervous system

Cooper, Maren, Bergsund, Marie M., Owens, Elizabeth, Powell, Daniel J., Berner, Emily, Janmohamed, Rania, Newstein, Peter, Dickinson, Patsy S.

2023

Overview

Changes in ambient temperature affect all biological processes. However, these effects are process specific and often vary non-linearly. It is thus a non-trivial problem for neuronal circuits to maintain coordinated, functional output across a range of temperatures. The cardiac nervous systems in two species of decapod crustaceans, Homarus americanus and Cancer borealis , can maintain function across a wide but physiologically relevant temperature range. However, the processes that underlie temperature resilience in neuronal circuits and muscle systems are not fully understood. Here, we demonstrate that the non-isolated cardiac nervous system (i.e., the whole heart: neurons, effector organs, intrinsic feedback systems) in the American lobster, H. americanus , is more sensitive to warm temperatures than the isolated cardiac ganglion (CG) that controls the heartbeat. This was surprising as modulatory processes known to stabilize the output from the CG are absent when the ganglion is isolated. One source of inhibitory feedback in the intact cardiac neuromuscular system is nitric oxide (NO), which is released in response to heart contractions. We hypothesized that the greater temperature tolerance observed in the isolated CG is due to the absence of NO feedback. Here, we demonstrate that applying an NO donor to the isolated CG reduces its temperature tolerance. Similarly, we show that the NO synthase inhibitor L-nitroarginine (LNA) increases the temperature tolerance of the non-isolated nervous system. This is sufficient to explain differences in temperature tolerance between the isolated CG and the whole heart. However, in an intact lobster, the heart and CG are modulated by an array of endogenous peptides and hormones, many of which are positive regulators of the heartbeat. Many studies have demonstrated that excitatory modulators increase temperature resilience. However, this neuromuscular system is regulated by both excitatory and inhibitory peptide modulators. Perfusing SGRNFLRFamide, a FLRFamide-like peptide, through the heart increases the non-isolated nervous system’s tolerance to high temperatures. In contrast, perfusing myosuppressin, a peptide that negatively regulates the heartbeat frequency, decreases the temperature tolerance. Our data suggest that, in this nervous system, positive regulators of neural output increase temperature tolerance of the neuromuscular system, while modulators that decrease neural output decrease temperature tolerance.

• Publisher: Frontiers Research Foundation,Frontiers Media S.A
• Subject: Animals / cardiac ganglion / crash temperature / Crustaceans / Feedback / FMRFamide-like neuropeptide / Functional morphology / Heart / Heat resistance / High temperature / Homarus americanus / L-arginine / Muscle contraction / myosuppressin / Nervous system / Neuromodulation / Neuromuscular system / Neurons / Neuroscience / Nitric oxide / Nitric-oxide synthase / Pacemakers / Peptides / Physiology / Temperature / Temperature tolerance