Parallel Use of Two Behavioral Mechanisms for Chemotaxis in Caenorhabditis elegans

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116

The nematode Caenorhabditis elegans navigates toward a preferred temperature setpoint (T s ) determined by long-term temperature exposure. During thermotaxis, the worm migrates down temperature gradients at temperatures above T s (negative thermotaxis) and performs isothermal tracking near T s . Under some conditions, the worm migrates up temperature gradients below T s (positive thermotaxis). Here, we analyze positive and negative thermotaxis toward T s to study the role of specific neurons that have been proposed to be involved in thermotaxis using genetic ablation, behavioral tracking, and calcium imaging. We find differences in the strategies for positive and negative thermotaxis. Negative thermotaxis is achieved through biasing the frequency of reorientation maneuvers (turns and reversal turns) and biasing the direction of reorientation maneuvers toward colder temperatures. Positive thermotaxis, in contrast, biases only the direction of reorientation maneuvers toward warmer temperatures. We find that the AFD thermosensory neuron drives both positive and negative thermotaxis. The AIY interneuron, which is postsynaptic to AFD, may mediate the switch from negative to positive thermotaxis below T s . We propose that multiple thermotactic behaviors, each defined by a distinct set of sensorimotor transformations, emanate from the AFD thermosensory neurons. AFD learns and stores the memory of preferred temperatures, detects temperature gradients, and drives the appropriate thermotactic behavior in each temperature regime by the flexible use of downstream circuits.N avigational behaviors provide a framework for exploring the interplay among sensorimotor circuits, learning, and memory. During a navigational task, animals eventually reach their goals by implementing strategies composed of sensorimotor rules. Experience can modify navigational goals, so memory can also be integrated into sensorimotor pathways. Studying navigation in the nematode Caenorhabditis elegans offers the possibility of understanding the plasticity and programming of sensorimotor circuits from input to output in a small nervous system (1).Previous studies established C. elegans thermotaxis as a model for experience-dependent navigation (2-6). When worms are exposed to specific temperatures between 15°C and 25°C for at least 4 h, they adopt those temperatures as their thermotactic setpoint (T s ) (2, 3, 5, 7). When placed on a spatial temperature gradient, worms seek the T s . When arriving near T s , worms track isotherms. Genetic analysis of thermotaxis has yielded mutants that are athermotactic (crawling randomly on temperature gradients), cryophilic (crawling to the coldest point on a temperature gradient irrespective of T s ), or thermophilic (crawling to the warmest point on a temperature gradient). This observation led to the suggestion that thermotaxis might involve separate circuits for negative thermotaxis (movement down gradients) and positive thermotaxis (movement up gradients) that balance near T s (2, 4).Systematic laser ablation a...

Section: Resultssupporting

confidence: 82%

“…Steering mechanisms (also called weathervaning) have been identified in C. elegans chemotaxis (11,21,22). To look for steering mechanisms, we focused on runs pointed orthogonally to the gradient.…”

Section: Resultsmentioning

confidence: 99%

Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

Luo

Cook

Venkatachalam

et al. 2014

100

116

“…Previous work has shown that worms use a klinokinesis strategy, where frequency of reversal is changed depending on the concentration of stimuli, when aerotaxing in the absence of food (29). This strategy resembles that used by worms chemotaxing to other cues such as salts and odors (26,30). Our quantitative experiments show that the URX oxygen sensors evoke reversals in response to O 2 stimuli that have only minor effects on speed.…”

Section: Discussionsupporting

confidence: 54%

Modulation of sensory information processing by a neuroglobin in Caenorhabditis elegans

Oda

Toyoshima

Bono

2017

T he response properties of sensory neurons can be characterized by tuning curves that relate stimulus parameters to the evoked response (1, 2). Some sensory neurons show dynamic ranges that span several orders of stimulus magnitude (e.g., odor concentration), whereas others show remarkably narrow tuning curves. For example, glomus cells of the carotid body show oxygenevoked responses that are tuned to a twofold to threefold change in O 2 levels at the physiologically appropriate O 2 concentration range (3, 4). How such sharp tuning is achieved is poorly understood.Neuroglobins are members of the globin family of hemebinding proteins expressed mainly in neurons (5). They have been described throughout metazoa, from cnidarians to man (6). Their physiological functions are unclear. They have been proposed to metabolize reactive oxygen species (ROS), signal redox state, store O 2 , control apoptosis, and negatively regulate Gi/o signaling (7). The genome of Caenorhabditis elegans encodes an unusually large family of globins, and many are expressed in neurons (8). One of these, GLOBIN-5 (GLB-5), is expressed in the oxygen sensing neurons URX, AQR, PQR, and BAG, where it accumulates at dendritic endings (9, 10). C. elegans avoids both normoxia (21% O 2 ) and hypoxia (11). Avoidance of 21% O 2 enables the animal to escape the surface and is mediated by O 2 receptors, most importantly the glb-5-expressing URX, AQR, and PQR neurons (12). Like vertebrate neuroglobins, GLB-5 has the spectroscopic fingerprints of a hexa-coordinated heme iron and rapidly oxidizes to the ferric state in normoxia (9). The glb-5 gene is defective in the domesticated reference strain of C. elegans, N2 (Bristol), but natural isolates encode a functional allele, glb-5(Haw) (9, 10) (Haw refers to Hawaii, the geographical origin of the natural isolate in which this allele was first described). Behavioral and Ca 2+ imaging studies suggest that functional GLB-5 alters the properties of the O 2 receptors and C. elegans' O 2 responses (9, 10). However, how GLB-5 alters the representation of environmental information in these neurons leading to behavioral change is unknown.The URX O 2 receptors exhibit phasic-tonic signaling properties and, in response to changes in O 2 concentration, evoke both transient behavioral responses that are coupled to the rate of change of O 2 , dO 2 /dt, and more persistent behavioral responses coupled to O 2 levels (8, 13). The transient responses are reversals and turns that allow C. elegans to navigate O 2 gradients. The sustained responses involve persistent changes in the rate of movement that enable feeding animals to escape 21% O 2 or to accumulate in preferred lower O 2 environments. Besides GLB-5, the URX neurons express another putative molecular O 2 sensor, a soluble guanylate cyclase composed of GCY-35 and GCY-36 (guanylate cyclase) subunits (11,13,14). These soluble guanylate cyclases have a heme-nitric oxide/oxygen (H-NOX) binding domain that appears to stimulate cGMP production upon binding molecular O 2 (10, ...

“…1D and Movie S1). These combined strategies would allow C. elegans to move efficiently to its preferred humidity level (16,17). In contrast, control worms assayed in the absence of a humidity gradient (with both troughs empty) showed no preference (Fig.…”

Section: Significancementioning

confidence: 99%

Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans

Russell

Vidal-Gadea

Makay

et al. 2014

All terrestrial animals must find a proper level of moisture to ensure their health and survival. The cellular-molecular basis for sensing humidity is unknown in most animals, however. We used the model nematode Caenorhabditis elegans to uncover a mechanism for sensing humidity. We found that whereas C. elegans showed no obvious preference for humidity levels under standard culture conditions, worms displayed a strong preference after pairing starvation with different humidity levels, orienting to gradients as shallow as 0.03% relative humidity per millimeter. Cell-specific ablation and rescue experiments demonstrate that orientation to humidity in C. elegans requires the obligatory combination of distinct mechanosensitive and thermosensitive pathways. The mechanosensitive pathway requires a conserved DEG/ENaC/ ASIC mechanoreceptor complex in the FLP neuron pair. Because humidity levels influence the hydration of the worm's cuticle, our results suggest that FLP may convey humidity information by reporting the degree that subcuticular dendritic sensory branches of FLP neurons are stretched by hydration. The thermosensitive pathway requires cGMP-gated channels in the AFD neuron pair. Because humidity levels affect evaporative cooling, AFD may convey humidity information by reporting thermal flux. Thus, humidity sensation arises as a metamodality in C. elegans that requires the integration of parallel mechanosensory and thermosensory pathways. This hygrosensation strategy, first proposed by Thunberg more than 100 y ago, may be conserved because the underlying pathways have cellular and molecular equivalents across a wide range of species, including insects and humans. mechanosensation | thermosensation M oisture is essential for life. As such, many animals have adapted different behavioral mechanisms to migrate toward their preferred moisture level (hygrotaxis) (1-6). For instance, Drosophila avoid high humidity that impedes flight, whereas green frogs orient toward high humidity to maintain hydration (5, 6). Animals also sense moisture levels to determine important information about their environment; for example, moths detect humidity levels around flowers to deduce which ones might be damaged and contain less nectar (7). These behaviors are often critical to keep an animal within its niche and regulate essential processes such as growth and reproduction. Thus, it is surprising that the molecular basis for how different humidity levels are detected and encoded by the nervous system (hygrosensation) remains unknown in most animals.The search for humidity receptors has achieved the most progress in insects. For instance, distinct sets of hygrosensitive neurons have been found in dome-shaped organs on the antenna of the giant cockroach (8). One set activates with moist air, and the other set responds to dry air. Similar moist and dry receptive neurons have been detected in the branched arista subsegment of the antennae in adult Drosophila (9). Removal of the arista or deletion of any one of three TRP channels expres...