Reconstruction of Spatial Thermal Gradient Encoded in Thermosensory Neuron AFD inCaenorhabditis elegans

Abstract

During navigation, animals process temporal sequences of sensory inputs to evaluate the surrounding environment. Thermotaxis of Caenorhabditis elegans is a favorable sensory behavior to elucidate how navigating animals process sensory signals from the environment. Sensation and storage of temperature information by a bilaterally symmetric pair of thermosensory neurons, AFD, is essential for the animals to migrate toward the memorized temperature on a thermal gradient. However, the encoding mechanisms of the spatial environment with the temporal AFD activity during navigation remain to be elucidated. Here, we show how the AFD neuron encodes sequences of sensory inputs to perceive spatial thermal environment. We used simultaneous calcium imaging and tracking system for a freely moving animal and characterized the response property of AFD to the thermal stimulus during thermotaxis. We show that AFD neurons respond to shallow temperature increases with intermittent calcium pulses and detect temperature differences with a critical time window of 20 s, which is similar to the timescale of behavioral elements of C. elegans, such as turning. Convolution of a thermal stimulus and the identified response property successfully reconstructs AFD activity. Conversely, deconvolution of the identified response kernel and AFD activity reconstructs the shallow thermal gradient with migration trajectory, indicating that AFD activity and the migration trajectory are sufficient as the encoded signals for thermal environment. Our study demonstrates bidirectional transformation between environmental thermal information and encoded neural activity.Key words: C. elegans; imaging; reconstruction; response function; thermosensory neuron; tracking IntroductionEvaluation of the surrounding environment is a vital ability for living organisms. When animals migrate through their environment, sensory systems convert external information into neural activities as temporally encoded signals. Depending on the encoded signals, animals organize sequences of movement with proper timing to migrate to preferred environments. Elucidating the neuronal mechanisms by which temporal activities of sensory neurons generated a response to environmental input is crucial for understanding the neural code to express and convey the Received July 28, 2015; revised Dec. 12, 2015; accepted Dec. 31, 2015. Author contributions: Y.T., H.N., S.I., and I. Significance StatementDeciphering how information is encoded in the nervous system is an important challenge for understanding the principles of information processing in neural circuits. During navigation behavior, animals transform spatial information to temporal patterns of neural activity. To elucidate how a sensory system achieves this transformation, we focused on a thermosensory neuron in Caenorhabditis elegans called AFD, which plays a major role in a sensory behavior. Using tracking and calcium imaging system for freely moving animals, we identified the response property of the AFD. The identified response pr...

A Calcium- and Diacylglycerol-Stimulated Protein Kinase C (PKC), Caenorhabditis elegans PKC-2, Links Thermal Signals to Learned Behavior by Acting in Sensory Neurons and Intestinal Cells

“…Second, after locating the T c , cryophilic migration ceases and animals track precisely along the T c within the gradient. The AFD sensory neuron is the principal receiver, encoder, and transducer of ambient temperature changes in C. elegans (22,25,27). Signals generated in AFD are transmitted to the postsynaptic AIY interneuron and indirectly to secondary interneurons for processing and integration.…”

“…Candidate and AWC neurons suggested that PKC-2 is involved in thermotaxis. AFD directly mediates temperature perception and controls a circuit that governs thermotaxis (25,27). AWC principally mediates responses to odorants (28).…”

Two New FRET Imaging Measures: Linearly Proportional to and Highly Contrasting the Fraction of Active Molecules

“…Because the mathematical models in these studies usually describe changes in the concentrations of signaling molecules, the LP measure should be useful for comparisons of simulations and experiments. In the computational data analyses of FRET imaging, dynamical relationships between molecular activity and certain biological outputs, e.g., membrane protrusion in our example ( Fig 4 ), have been examined via cross-correlation analysis [27, 31, 32], and intracellular signal transfer from the molecular activity to the biological output has been identified as the response function [33, 34]. In these analyses, the LP measure could be favorable for avoiding signals that are biasedly amplified by the ratiometric measure ( Fig 3D ).…”

Molecules empowering animals to sense and respond to temperature in changing environments

“…This was demonstrated by Kobayashi and collaborators, showing that cultured AFD neurons harbor all of the necessary machinery to store and update a thermal memory [42 ], although ex vivo responses were more variable than in vivo responses. In another study, the same group showed that in worms navigating in a continuous temperature gradient, the combination of motion-imposed thermal variations and short-term adaptation properties produced intermittent activity peaks in AFD [43]. Discrete AFD activity events correlated with turns in well-fed, but not starved animals.…”

“…However, it seems that FLP in cmk-1 mutants has at least superficially intact thermo-detection abilities and that CMK-1 signaling might rather adjust the nature or the degree of neurotransmission to secondary neurons. This situation might be reminiscent of the apparent uncoupling between thermosensation and behavior observed upon starvation in AFD [43]. …”