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Life on Earth evolved under a specific set of environmental conditions, including consistent gravitational and magnetic fields. However, planned human missions to Mars in the coming decades will expose terrestrial organisms to radically different conditions, with Martian gravity being approximately 38% of Earth's and a significantly reduced magnetic field. Understanding the combined effects of these factors is crucial, as they may impact biological systems that evolved under different conditions. In this study, we investigated the effects of simulated Martian gravity and hypomagnetic fields on the nematode Caenorhabditis elegans across six generations. We used an integrated experimental setup consisting of clinostats to mimic the reduced Martian gravity, and Merritt coil magnetic cages to model the decreased Martian magnetic fields. We assessed behavioral, morphological, and physiological responses of C. elegans. High-throughput automated assays revealed significant reductions in motor output and morphological dimensions for animals in the Mars treatment compared to matched earth-like controls. We assessed neurological function by means of chemotaxis assays and found a progressive decline in performance for worms raised under the Martian paradigm compared to Earth controls. Our results show that worms grown under Martian-like conditions exhibit progressive physiological alterations across generations, suggesting that the unique environment of Mars might pose challenges to biological function and adaptation. These findings contribute to understanding how living organisms may respond to the combined effects of reduced gravity and hypomagnetic fields, providing insights relevant for future human exploration and potential colonization of Mars. 

Mechanosensitive PIEZO ion channels are evolutionarily conserved proteins that are widely expressed in neuronal and muscular tissues. This study explores the role of the mechanoreceptor PEZO-1 in the body wall muscles of Caenorhabditis elegans, focusing on its influence on two locomotor behaviors, swimming and crawling. Using confocal imaging, we reveal that PEZO-1 localizes to the sarcolemma and plays a crucial role in modulating calcium dynamics that are important for muscle contraction. When we knocked down pezo-1 expression in striated muscles with RNA interference, calcium levels in head and tail muscles increased. While heightened, the overall trajectory of the calcium signal during the crawl cycle remained the same. While downregulation of pezo-1 led to an increase in crawling speed, it caused a reduction in swimming speed. Reduction in pezo-1 expression also resulted in the increased activation of the ventral tail muscles, and a disruption of dorsoventral movement asymmetry, a critical feature that enables propulsion in water. These alterations were correlated with impaired swimming posture and path curvature, suggesting that PEZO-1 has different functions during swimming and crawling. 

The discovery in 2010 of the PIEZO family of mechanoreceptors revolutionized our understanding of the role of proprioceptive feedback in mammalian physiology. Much remains to be elucidated. This study looks at the role this receptor plays in normal locomotion. Like humans, the nematode C. elegans expresses PIEZO-type channels (encoded by the pezo-1 gene) throughout its somatic musculature. Here we use the unbiased automated behavioral software Tierpsy to characterize the effects that mutations removing PEZO-1 from body wall musculature have on C. elegans crawling. We find that loss of PEZO-1 results in disrupted locomotion and posture, consistent with phenotypes associated with loss of PIEZO2 in human musculature. C. elegans is thus an amenable system to study the role of mechanoreception on muscle physiology and function. 

Abstract Once considered mere structural support cells in the nervous system, glia have recently been demonstrated to play pivotal roles in sensorimotor processing and to directly respond to sensory stimuli. However, their response properties and contributions to sensory-induced behaviors remain little understood. InCaenorhabditis elegans, the amphid sheath glia (AMsh) directly respond to aversive odorants and mechanical stimuli, but their precise transduction machinery and their behavioral relevance remain unclear. We investigated the role of AMsh in mechanosensation and their impact on escape behaviors inC. elegans. We found that nose touch stimuli in immobilized animals induced a slow calcium wave in AMsh, which coincided with the termination of escape reversal behaviors. Genetic ablation of AMsh resulted in prolonged reversal durations in response to nose touch, but not to harsh anterior touch, highlighting the specificity of AMsh’s role in distinct escape behaviors. Mechanotransduction in AMsh requires the α-tubulin MEC-12 and the ion channels ITR-1 and OSM-9, indicating a unique mechanosensory pathway that is distinct from the neighboring ASH neurons. We find that GABAergic signaling mediated by the GABA-A receptor orthologs LGC-37/8 and UNC-49 play a crucial role in modulating the duration of nose touch-induced reversals. We conclude that in addition to aversive odorant detection, AMsh mediate mechanosensation, play a pivotal role in terminating escape responses to nose touch, and provide a mechanism to maintain high sensitivity to polymodal sensory stimuli. SignificancePolymodal nociceptive sensory neurons have the challenge of multitasking across sensory modalities. They must respond to dangerous stimuli of one modality, but also adapt to repeated nonthreatening stimuli without compromising sensitivity to harmful stimuli from different modalities. Here we show that a pair of glia in the nematodeC. elegansmodulate the duration of nose-touch induced escape responses. We identify several molecules involved in the transduction of mechanical stimuli in these cells and show that they use the signaling molecule GABA to modulate neural function. We propose a mechanism through which these glia might function to maintain this polysensory neuron responsive to dangerous stimuli across different modalities. 

IntroductionAt the cellular level, acute temperature changes alter ionic conductances, ion channel kinetics, and the activity of entire neuronal circuits. This can result in severe consequences for neural function, animal behavior and survival. In poikilothermic animals, and particularly in aquatic species whose core temperature equals the surrounding water temperature, neurons experience rather rapid and wide-ranging temperature fluctuations. Recent work on pattern generating neural circuits in the crustacean stomatogastric nervous system have demonstrated that neuronal circuits can exhibit an intrinsic robustness to temperature fluctuations. However, considering the increased warming of the oceans and recurring heatwaves due to climate change, the question arises whether this intrinsic robustness can acclimate to changing environmental conditions, and whether it differs between species and ocean habitats. MethodsWe address these questions using the pyloric pattern generating circuits in the stomatogastric nervous system of two crab species,Hemigrapsus sanguineusandCarcinus maenasthat have seen a worldwide expansion in recent decades. Results and discussionConsistent with their history as invasive species, we find that pyloric activity showed a broad temperature robustness (>30°C). Moreover, the temperature-robust range was dependent on habitat temperature in both species. Warm-acclimating animals shifted the critical temperature at which circuit activity breaks down to higher temperatures. This came at the cost of robustness against cold stimuli inH. sanguineus, but not inC. maenas. Comparing the temperature responses ofC. maenasfrom a cold latitude (the North Sea) to those from a warm latitude (Spain) demonstrated that similar shifts in robustness occurred in natural environments. Our results thus demonstrate that neuronal temperature robustness correlates with, and responds to, environmental temperature conditions, potentially preparing animals for changing ecological conditions and shifting habitats. 

In this work, we study the interplay between chaos and noise in neuronal state transitions involving period doubling cascades. Our approach involves the implementation of a neuronal mathematical model under the action of neuromodulatory input, with and without noise, as well as equivalent experimental work on a biological neuron in the stomatogastric ganglion of the crab Cancer borealis. Our simulations show typical transitions between tonic and bursting regimes that are mediated by chaos and period doubling cascades. While this transition is less evident when intrinsic noise is present in the model, the noisy computational output displays features akin to our experimental results. The differences and similarities observed in the computational and experimental approaches are discussed. 

Acute temperature changes can disrupt neuronal activity and coordination with severe consequences for animal behavior and survival. Nonetheless, two rhythmic neuronal circuits in the crustacean stomatogastric ganglion (STG) and their coordination are maintained across a broad temperature range. However, it remains unclear how this temperature robustness is achieved. Here, we dissociate temperature effects on the rhythm generating circuits from those on upstream ganglia. We demonstrate that heat-activated factors extrinsic to the rhythm generators are essential to the slow gastric mill rhythm’s temperature robustness and contribute to the temperature response of the fast pyloric rhythm. The gastric mill rhythm crashed when its rhythm generator in the STG was heated. It was restored when upstream ganglia were heated and temperature-matched to the STG. This also increased the activity of the peptidergic modulatory projection neuron (MCN1), which innervates the gastric mill circuit. Correspondingly, MCN1’s neuropeptide transmitter stabilized the rhythm and maintained it over a broad temperature range. Extrinsic neuromodulation is thus essential for the oscillatory circuits in the STG and enables neural circuits to maintain function in temperature-compromised conditions. In contrast, integer coupling between pyloric and gastric mill rhythms was independent of whether extrinsic inputs and STG pattern generators were temperature-matched or not, demonstrating that the temperature robustness of the coupling is enabled by properties intrinsic to the rhythm generators. However, at near-crash temperature, integer coupling was maintained only in some animals while it was absent in others. This was true despite regular rhythmic activity in all animals, supporting that degenerate circuit properties result in idiosyncratic responses to environmental challenges. 

For over a century the nervous system of decapod crustaceans has been a workhorse for the neurobiology community. Many fundamental discoveries including the identification of electrical and inhibitory synapses, lateral and pre-synaptic inhibition, and the Na + /K + -pump were made using lobsters, crabs, or crayfish. Key among many advantages of crustaceans for neurobiological research is the unique access to large, accessible, and identifiable neurons, and the many distinct and complex behaviors that can be observed in lab settings. Despite these advantages, recent decades have seen work on crustaceans hindered by the lack of molecular and genetic tools required for unveiling the cellular processes contributing to neurophysiology and behavior. In this perspective paper, we argue that the recently sequenced marbled crayfish, Procambarus virginalis , is suited to become a genetic model system for crustacean neuroscience. P. virginalis are parthenogenetic and produce genetically identical offspring, suggesting that germline transformation creates transgenic animal strains that are easy to maintain across generations. Like other decapod crustaceans, marbled crayfish possess large neurons in well-studied circuits such as the giant tail flip neurons and central pattern generating neurons in the stomatogastric ganglion. We provide initial data demonstrating that marbled crayfish neurons are accessible through standard physiological and molecular techniques, including single-cell electrophysiology, gene expression measurements, and RNA-interference. We discuss progress in CRISPR-mediated manipulations of the germline to knock-out target genes using the ‘Receptor-mediated ovary transduction of cargo’ (ReMOT) method. Finally, we consider the impact these approaches will have for neurophysiology research in decapod crustaceans and more broadly across invertebrates. 

Like their chemical counterparts, electrical synapses show complex dynamics such as rectification and voltage dependence that interact with other electrical processes in neurons. The consequences arising from these interactions for the electrical behavior of the synapse, and the dynamics they create, remain largely unexplored. Using a voltage-dependent electrical synapse between a descending modulatory projection neuron (MCN1) and a motor neuron (LG) in the crustacean stomatogastric ganglion, we find that the influence of the hyperpolarization-activated inward current ( I h ) is critical to the function of the electrical synapse. When we blocked I h with CsCl, the apparent voltage dependence of the electrical synapse shifted by 18.7 mV to more hyperpolarized voltages, placing the dynamic range of the electrical synapse outside of the range of voltages used by the LG motor neuron (−60.2 mV to −44.9 mV). With dual electrode current- and voltage-clamp recordings, we demonstrate that this voltage shift is not due to a change in the properties of the gap junction itself, but is a result of a sustained effect of I h on the presynaptic MCN1 axon terminal membrane potential. I h -induced depolarization of the axon terminal membrane potential increased the electrical postsynaptic potentials and currents. With I h present, the axon terminal resting membrane potential is depolarized, shifting the dynamic range of the electrical synapse toward the functional range of the motor neuron. We thus demonstrate that the function of an electrical synapse is critically influenced by a voltage-dependent ionic current ( I h ). NEW & NOTEWORTHY Electrical synapses and voltage-gated ionic currents are often studied independently from one another, despite mounting evidence that their interactions can alter synaptic behavior. We show that the hyperpolarization-activated inward ionic current shifts the voltage dependence of electrical synaptic transmission through its depolarizing effect on the membrane potential, enabling it to lie within the functional membrane potential range of a motor neuron. Thus, the electrical synapse’s function critically depends on the voltage-gated ionic current.