Thermotactic behaviour in lacustrine and riverine forms of Salmo trutta and its relevance to an emerging parasitic disease (PKD) in the wake of climate change.

The thermotactic response of brown trout (Salmo trutta) was examined with the goal to investigate potential effects of the emerging temperature-dependent fatal trout disease PKD (proliferative kidney disease). First the differences in cold-water preferences of two forms of brown trout, lacustrine (migratory) and riverine, were determined. Second, it was studied whether this preference was changed in fish infected with PKD. The experiment involved a one-week habituation period at 14 °C in a two-chamber runway followed by a week of 3 °C temperature difference between the two runways. The fish could freely move between lanes via an opening at the end where food was provided. The temperature manipulation was repeated twice, and there were 3 trials per experimental group. All fish developed a clear spatial preference in the test. Lacustrine trout demonstrated a preference for warmer water, while riverine trout preferred cooler water. This may increase the risk to PKD in the lacustrine form. Most strikingly, riverine trout experimentally exposed to Tetracapsuloides bryosalmonae, the parasite that causes PKD, demonstrated stronger cold-seeking behaviour than control fish. Cold seeking behaviour suggests the occurrence of a disease-induced behavioural chill response, which may play an important role in disease recovery. This demonstrates the significance of protecting river connectivity and cold-water sanctuaries as management strategies for preserving salmonid populations in a warming climate.

Optimal Control of Collective Electrotaxis in Epithelial Monolayers.

Epithelial monolayers are some of the best-studied models for collective cell migration due to their abundance in multicellular systems and their tractability. Experimentally, the collective migration of epithelial monolayers can be robustly steered e.g. using electric fields, via a process termed electrotaxis. Theoretically, however, the question of how to design an electric field to achieve a desired spatiotemporal movement pattern is underexplored. In this work, we construct and calibrate an ordinary differential equation model to predict the average velocity of the centre of mass of a cellular monolayer in response to stimulation with an electric field. We use this model, in conjunction with optimal control theory, to derive physically realistic optimal electric field designs to achieve a variety of aims, including maximising the total distance travelled by the monolayer, maximising the monolayer velocity, and keeping the monolayer velocity constant during stimulation. Together, this work is the first to present a unified framework for optimal control of collective monolayer electrotaxis and provides a blueprint to optimally steer collective migration using other external cues.

A hyperpolarizing neuron recruits undocked innexin hemichannels to transmit neural information in Caenorhabditis elegans.

While depolarization of the neuronal membrane is known to evoke the neurotransmitter release from synaptic vesicles, hyperpolarization is regarded as a resting state of chemical neurotransmission. Here, we report that hyperpolarizing neurons can actively signal neural information by employing undocked hemichannels. We show that UNC-7, a member of the innexin family in Caenorhabditis elegans, functions as a hemichannel in thermosensory neurons and transmits temperature information from the thermosensory neurons to their postsynaptic interneurons. By monitoring neural activities in freely behaving animals, we find that hyperpolarizing thermosensory neurons inhibit the activity of the interneurons and that UNC-7 hemichannels regulate this process. UNC-7 is required to control thermotaxis behavior and functions independently of synaptic vesicle exocytosis. Our findings suggest that innexin hemichannels mediate neurotransmission from hyperpolarizing neurons in a manner that is distinct from the synaptic transmission, expanding the way of neural circuitry operations.

Uncommon opsin's retinal isomer is involved in mammalian sperm thermotaxis.

In recent years it became apparent that, in mammals, rhodopsin and other opsins, known to act as photosensors in the visual system, are also present in spermatozoa, where they function as highly sensitive thermosensors for thermotaxis. The intriguing question how a well-conserved protein functions as a photosensor in one type of cells and as a thermosensor in another type of cells is unresolved. Since the moiety that confers photosensitivity on opsins is the chromophore retinal, we examined whether retinal is substituted in spermatozoa with a thermosensitive molecule. We found by both functional assays and mass spectrometry that retinal is present in spermatozoa and required for thermotaxis. Thus, starvation of mice for vitamin A (a precursor of retinal) resulted in loss of sperm thermotaxis, without affecting motility and the physiological state of the spermatozoa. Thermotaxis was restored after replenishment of vitamin A. Using reversed-phase ultra-performance liquid chromatography mass spectrometry, we detected the presence of retinal in extracts of mouse and human spermatozoa. By employing UltraPerformance convergence chromatography, we identified a unique retinal isomer in the sperm extracts-tri-cis retinal, different from the photosensitive 11-cis isomer in the visual system. The facts (a) that opsins are thermosensors for sperm thermotaxis, (b) that retinal is essential for thermotaxis, and (c) that tri-cis retinal isomer uniquely resides in spermatozoa and is relatively thermally unstable, suggest that tri-cis retinal is involved in the thermosensing activity of spermatozoa.

Thermotaxis of mammalian sperm.

Sperm are guided through the female reproductive tract. A temperature difference of about 2°C exists between the storage site and fertilization site of the mammalian oviduct, leading to the hypothesis that sperm can sense and swim towards the oocyte along a rising temperature gradient, known as thermotaxis. Research over the past two decades has reported that sperm feature a sophisticated thermal detection system to detect and track ambient temperature gradients. More recently, thermotaxis is expected to be added to the microfluidic isolation method based on sperm tactic responses for sperm selection. In this article, mammalian sperm thermotaxis is discussed, explaining the underlying behavioural mechanisms and molecular basis, according to the latest research. Finally, this article explores the possible application of sperm thermotaxis in ART.

Environmental-temperature and internal-state dependent thermotaxis plasticity of nematodes.

Thermotaxis behavior of Caenorhabditis elegans is robust and highly plastic. A pair of sensory neurons, AFD, memorize environmental/cultivation temperature and communicate with a downstream neural circuit to adjust the temperature preference of the animal. This results in a behavioral bias where worms will move toward their cultivation temperature on a thermal gradient. Thermotaxis of C. elegans is also affected by the internal state and is temporarily abolished when worms are starved. Here I will discuss how C. elegans is able to modulate its behavior based on temperature by integrating environmental and internal information. Recent studies show that some parasitic nematodes have a similar thermosensory mechanism to C. elegans and exhibit cultivation-temperature-dependent thermotaxis. I will also discuss the common neural mechanisms that regulate thermosensation and thermotaxis in C. elegans and Strongyloides stercoralis.

Fluidic bacterial diodes rectify magnetotactic cell motility in porous environments.

Directed motility enables swimming microbes to navigate their environment for resources via chemo-, photo-, and magneto-taxis. However, directed motility competes with fluid flow in porous microbial habitats, affecting biofilm formation and disease transmission. Despite this broad importance, a microscopic understanding of how directed motility impacts the transport of microswimmers in flows through constricted pores remains unknown. Through microfluidic experiments, we show that individual magnetotactic bacteria directed upstream through pores display three distinct regimes, whereby cells swim upstream, become trapped within a pore, or are advected downstream. These transport regimes are reminiscent of the electrical conductivity of a diode and are accurately predicted by a comprehensive Langevin model. The diode-like behavior persists at the pore scale in geometries of higher dimension, where disorder impacts conductivity at the sample scale by extending the trapping regime over a broader range of flow speeds. This work has implications for our understanding of the survival strategies of magnetotactic bacteria in sediments and for developing their use in drug delivery applications in vascular networks.

Environmental conditions, diel period, and fish size influence the horizontal and vertical movements of red snapper.

Most demersal fishes are difficult to observe and track due to methodological and analytical constraints. We used an acoustic positioning system to elucidate the horizontal and vertical movements of 44 red snapper (Lutjanus campechanus) off North Carolina, USA, in 2019. Mean movement rate and distance off bottom varied by individual, with larger red snapper generally moving faster and spending more time farther off the bottom than smaller individuals. We used generalized additive mixed models that accounted for temporal autocorrelation in the data to show that mean hourly red snapper movement rate was lower during the day than at night and was negatively related to bottom water temperature. Moreover, red snapper spent more time off the bottom during the day than at night, and vertical movements were mostly related to bottom upwelling events that sporadically occurred in May-July. Our results and previous observations suggest that red snapper feed primarily on benthic organisms at night, and display diel vertical migration (i.e., thermotaxis) up to warmer waters (when present) during the day to aid digestive efficiency. Movement is a central organizing feature in ecology, and the sustainable management of fish will benefit from a better understanding of the timing and causes of fish movement.

Robustness and plasticity in Drosophila heat avoidance.

Simple innate behavior is often described as hard-wired and largely inflexible. Here, we show that the avoidance of hot temperature, a simple innate behavior, contains unexpected plasticity in Drosophila. First, we demonstrate that hot receptor neurons of the antenna and their molecular heat sensor, Gr28B.d, are essential for flies to produce escape turns away from heat. High-resolution fly tracking combined with a 3D simulation of the thermal environment shows that, in steep thermal gradients, the direction of escape turns is determined by minute temperature differences between the antennae (0.1°-1 °C). In parallel, live calcium imaging confirms that such small stimuli reliably activate both peripheral thermosensory neurons and central circuits. Next, based on our measurements, we evolve a fly/vehicle model with two symmetrical sensors and motors (a "Braitenberg vehicle") which closely approximates basic fly thermotaxis. Critical differences between real flies and the hard-wired vehicle reveal that fly heat avoidance involves decision-making, relies on rapid learning, and is robust to new conditions, features generally associated with more complex behavior.

C. elegans electrotaxis behavior is modulated by heat shock response and unfolded protein response signaling pathways.

The nematode C. elegans is a leading model to investigate the mechanisms of stress-induced behavioral changes coupled with biochemical mechanisms. Our group has previously characterized C. elegans behavior using a microfluidic-based electrotaxis device, and showed that worms display directional motion in the presence of a mild electric field. In this study, we describe the effects of various forms of genetic and environmental stress on the electrotactic movement of animals. Using exposure to chemicals, such as paraquat and tunicamycin, as well as mitochondrial and endoplasmic reticulum (ER) unfolded protein response (UPR) mutants, we demonstrate that chronic stress causes abnormal movement. Additionally, we report that pqe-1 (human RNA exonuclease 1 homolog) is necessary for the maintenance of multiple stress response signaling and electrotaxis behavior of animals. Further, exposure of C. elegans to several environmental stress-inducing conditions revealed that while chronic heat and dietary restriction caused electrotaxis speed deficits due to prolonged stress, daily exercise had a beneficial effect on the animals, likely due to improved muscle health and transient activation of UPR. Overall, these data demonstrate that the electrotaxis behavior of worms is susceptible to cytosolic, mitochondrial, and ER stress, and that multiple stress response pathways contribute to its preservation in the face of stressful stimuli.

Collective dynamics in entangled worm and robot blobs.

Living systems at all scales aggregate in large numbers for a variety of functions including mating, predation, and survival. The majority of such systems consist of unconnected individuals that collectively flock, school, or swarm. However, some aggregations involve physically entangled individuals, which can confer emergent mechanofunctional material properties to the collective. Here, we study in laboratory experiments and rationalize in theoretical and robophysical models the dynamics of physically entangled and motile self-assemblies of 1-cm-long California blackworms (Lumbriculus variegatus, Annelida: Clitellata: Lumbriculidae). Thousands of individual worms form braids with their long, slender, and flexible bodies to make a three-dimensional, soft, and shape-shifting "blob." The blob behaves as a living material capable of mitigating damage and assault from environmental stresses through dynamic shape transformations, including minimizing surface area for survival against desiccation and enabling transport (negative thermotaxis) from hazardous environments (like heat). We specifically focus on the locomotion of the blob to understand how an amorphous entangled ball of worms can break symmetry to move across a substrate. We hypothesize that the collective blob displays rudimentary differentiation of function across itself, which when combined with entanglement dynamics facilitates directed persistent blob locomotion. To test this, we develop a robophysical model of the worm blobs, which displays emergent locomotion in the collective without sophisticated control or programming of any individual robot. The emergent dynamics of the living functional blob and robophysical model can inform the design of additional classes of adaptive mechanofunctional living materials and emergent robotics.

Persistent thermal input controls steering behavior in Caenorhabditis elegans.

Motile organisms actively detect environmental signals and migrate to a preferable environment. Especially, small animals convert subtle spatial difference in sensory input into orientation behavioral output for directly steering toward a destination, but the neural mechanisms underlying steering behavior remain elusive. Here, we analyze a C. elegans thermotactic behavior in which a small number of neurons are shown to mediate steering toward a destination temperature. We construct a neuroanatomical model and use an evolutionary algorithm to find configurations of the model that reproduce empirical thermotactic behavior. We find that, in all the evolved models, steering curvature are modulated by temporally persistent thermal signals sensed beyond the time scale of sinusoidal locomotion of C. elegans. Persistent rise in temperature decreases steering curvature resulting in straight movement of model worms, whereas fall in temperature increases curvature resulting in crooked movement. This relation between temperature change and steering curvature reproduces the empirical thermotactic migration up thermal gradients and steering bias toward higher temperature. Further, spectrum decomposition of neural activities in model worms show that thermal signals are transmitted from a sensory neuron to motor neurons on the longer time scale than sinusoidal locomotion of C. elegans. Our results suggest that employments of temporally persistent sensory signals enable small animals to steer toward a destination in natural environment with variable, noisy, and subtle cues.

Vascular endothelial and smooth muscle cell galvanotactic response and differential migratory behavior.

Chronic disease or injury of the vasculature impairs the functionality of vascular wall cells particularly in their ability to migrate and repair vascular surfaces. Under pathologic conditions, vascular endothelial cells (ECs) lose their non-thrombogenic properties and decrease their motility. Alternatively, vascular smooth muscle cells (SMCs) may increase motility and proliferation, leading to blood vessel luminal invasion. Current therapies to prevent subsequent blood vessel occlusion commonly mechanically injure vascular cells leading to endothelial denudation and smooth muscle cell luminal migration. Due to this dichotomous migratory behavior, a need exists for modulating vascular cell growth and migration in a more targeted manner. Here, we examine the efficacy of utilizing small direct current electric fields to influence vascular cell-specific migration ("galvanotaxis"). We designed, fabricated, and implemented an in vitro chamber for tracking vascular cell migration direction, distance, and displacement under galvanotactic influence of varying magnitude. Our results indicate that vascular ECs and SMCs have differing responses to galvanotaxis; ECs exhibit a positive correlation of anodal migration while SMCs exhibit minimal change in directional migration in relation to the electric field direction. SMCs exhibit less motility response (i.e. distance traveled in 4 h) compared to ECs, but SMCs show a significantly higher motility at low electric potentials (80 mV/cm). With further investigation and translation, galvanotaxis may be an effective solution for modulation of vascular cell-specific migration, leading to enhanced endothelialization, with coordinate reduced smooth muscle in-migration.

Feeding state functionally reconfigures a sensory circuit to drive thermosensory behavioral plasticity.

Internal state alters sensory behaviors to optimize survival strategies. The neuronal mechanisms underlying hunger-dependent behavioral plasticity are not fully characterized. Here we show that feeding state alters C. elegans thermotaxis behavior by engaging a modulatory circuit whose activity gates the output of the core thermotaxis network. Feeding state does not alter the activity of the core thermotaxis circuit comprised of AFD thermosensory and AIY interneurons. Instead, prolonged food deprivation potentiates temperature responses in the AWC sensory neurons, which inhibit the postsynaptic AIA interneurons to override and disrupt AFD-driven thermotaxis behavior. Acute inhibition and activation of AWC and AIA, respectively, restores negative thermotaxis in starved animals. We find that state-dependent modulation of AWC-AIA temperature responses requires INS-1 insulin-like peptide signaling from the gut and DAF-16/FOXO function in AWC. Our results describe a mechanism by which functional reconfiguration of a sensory network via gut-brain signaling drives state-dependent behavioral flexibility.

Analysis of barotactic and chemotactic guidance cues on directional decision-making of Dictyostelium discoideum cells in confined environments.

Neutrophils and dendritic cells when migrating in confined environments have been shown to actuate a directional choice toward paths of least hydraulic resistance (barotaxis), in some cases overriding chemotactic responses. Here, we investigate whether this barotactic response is conserved in the more primitive model organism Dictyostelium discoideum using a microfluidic chip design. This design allowed us to monitor the behavior of single cells via live imaging when confronted with bifurcating microchannels, presenting different combinations of hydraulic and chemical stimuli. Under the conditions employed we find no evidence in support of a barotactic response; the cells base their directional choices on the chemotactic cues. When the cells are confronted by a microchannel bifurcation, they often split their leading edge and start moving into both channels, before a decision is made to move into one and retract from the other channel. Analysis of this decision-making process has shown that cells in steeper nonhydrolyzable adenosine- 3', 5'- cyclic monophosphorothioate, Sp- isomer (cAMPS) gradients move faster and split more readily. Furthermore, there exists a highly significant strong correlation between the velocity of the pseudopod moving up the cAMPS gradient to the total velocity of the pseudopods moving up and down the gradient over a large range of velocities. This suggests a role for a critical cortical tension gradient in the directional decision-making process.

Neuroethology of acoustic communication in field crickets - from signal generation to song recognition in an insect brain.

Field crickets are best known for the loud calling songs produced by males to attract conspecific females. This review aims to summarize the current knowledge of the neurobiological basis underlying the acoustic communication for mate finding in field crickets with emphasis on the recent research progress to understand the neuronal networks for motor pattern generation and auditory pattern recognition of the calling song in Gryllus bimaculatus. Strong scientific interest into the neural mechanisms underlying intraspecific communication has driven persistently advancing research efforts to study the male singing behaviour and female phonotaxis for mate finding in these insects. The growing neurobiological understanding also inspired many studies testing verifiable hypotheses in sensory ecology, bioacoustics and on the genetics and evolution of behaviour. Over last decades, acoustic communication in field crickets served as a very successful neuroethological model system. It has contributed significantly to the scientific process of establishing, reconsidering and refining fundamental concepts in behavioural neurosciences such as command neurons, central motor pattern generation, corollary discharge processing and pattern recognition by sensory feature detection, which are basic building blocks of our modern understanding on how nervous systems control and generate behaviour in all animals.

Durotaxis.

In this Primer, Sunyer and Trepat introduce durotaxis, the mode of migration by which cells follow gradients of extracellular matrix stiffness.

Temperature signaling underlying thermotaxis and cold tolerance in Caenorhabditis elegans.

Caenorhabditis elegans has a simple nervous system of 302 neurons. It however senses environmental cues incredibly precisely and produces various behaviors by processing information in the neural circuit. In addition to classical genetic analysis, fluorescent proteins and calcium indicators enable in vivo monitoring of protein dynamics and neural activity on either fixed or free-moving worms. These analyses have provided the detailed molecular mechanisms of neuronal and systemic signaling that regulate worm responses. Here, we focus on responses of C. elegans against temperature and review key findings that regulate thermotaxis and cold tolerance. Thermotaxis of C. elegans has been studied extensively for almost 50 years, and cold tolerance is a relatively recent concept in C. elegans. Although both thermotaxis and cold tolerance require temperature sensation, the responsible neurons and molecular pathways are different, and C. elegans uses the proper mechanisms depending on its situation. We summarize the molecular mechanisms of the major thermosensory circuit as well as the modulatory strategy through neural and tissue communication that enables fine tuning of thermotaxis and cold tolerance.

Searching for magnetic compass mechanism in pigeon retinal photoreceptors.

Migratory birds can detect the direction of the Earth's magnetic field using the magnetic compass sense. However, the sensory basis of the magnetic compass still remains a puzzle. A large body of indirect evidence suggests that magnetic compass in birds is localized in the retina. To confirm this point, an evidence of visual signals modulation by magnetic field (MF) should be obtained. In a previous study we showed that MF inclination impacts the amplitude of ex vivo electroretinogram (ERG) recorded from isolated pigeon retina. Here we present the results of an analysis of putative MF effect on one component of ERG, the photoreceptor's response, isolated from the total ERG by adding sodium aspartate and barium chloride to the perfusion solution. Photoresponses were recorded from isolated retinae of domestic pigeons Columba livia. The retinal samples were placed in MF that was modulated by three pairs of orthogonal Helmholtz coils. Light stimuli (blue and red) were applied under two inclinations of MF, 0° and 90°. In all the experiments, preparations from two parts of retina were used, red field (with dominant red-sensitive cones) and yellow field (with relatively uniform distribution of cone color types). In contrast to the whole retinal ERG, we did not observe any effect of MF inclination on either amplitude or kinetics of pharmacologically isolated photoreceptor responses to blue or red half-saturating flashes. A possible explanations of these results could be that magnetic compass sense is localized in retinal cells other than photoreceptors, or that photoreceptors do participate in magnetoreception, but require some processing of compass information in other retinal layers, so that only whole retina signal can reflect the response to changing MF.

The shape effect of flagella is more important than bottom-heaviness on passive gravitactic orientation in Chlamydomonas reinhardtii.

The way the unicellular, biflagellated, green alga Chlamydomonas orients upward has long been discussed in terms of both mechanics and physiology. In this study, we focus on the mechanics, i.e. the 'passive' mechanisms, of gravitaxis. To rotate the body upwards, cellular asymmetry is critical. Chlamydomonas can be depicted as a nearly spherical cell body with two anterior, symmetric flagella. The present study looks at the question of whether the existence of the flagella significantly affects torque generation in upward reorientation. The 'density asymmetry model' assumes that the cell is spherical and bottom-heavy and that the shape and weight of the flagella are negligible, while the 'shape asymmetry model' considers the shape of the flagella. Both our experimental and simulation results revealed a considerable contribution from shape asymmetry to the upward orientation of Chlamydomonas reinhardtii, which was several times larger than that of density asymmetry. From the experimental results, we also quantified the extent of bottom-heaviness, i.e. the distance between the centers of gravity and the figure when the cell body is assumed to be spherical. Our estimation was approximately 30 nm, only one-third of previous assumptions. These findings indicate the importance of the viscous drag of the flagella to the upward orientation, and thus negative gravitaxis, in Chlamydomonas.