Noriyuki Ohnishi

Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans

In complex neural circuits of the brain, massive information is processed with neuronal communication through synaptic transmissions. It is thus fundamental to delineate information flows encoded by various kinds of transmissions. Here, we show that glutamate signals from two distinct sensory neurons bidirectionally affect the same postsynaptic interneuron, thereby producing the opposite behaviours. EAT‐4/VGLUT (vesicular glutamate transporter)‐dependent glutamate signals from AFD thermosensory neurons inhibit the postsynaptic AIY interneurons through activation of GLC‐3/GluCl inhibitory glutamate receptor and behaviourally drive migration towards colder temperature. By contrast, EAT‐4‐dependent glutamate signals from AWC thermosensory neurons stimulate the AIY neurons to induce migration towards warmer temperature. Alteration of the strength of AFD and AWC signals led to significant changes of AIY activity, resulting in drastic modulation of behaviour. We thus provide an important insight on information processing, in which two glutamate transmissions encoding opposite information flows regulate neural activities to produce a large spectrum of behavioural outputs.

Neural coding in a single sensory neuron controlling opposite seeking behaviours in Caenorhabditis elegans

Unveiling the neural codes for intricate behaviours is a major challenge in neuroscience. The neural circuit for the temperature-seeking behaviour of Caenorhabditis elegans is an ideal system to dissect how neurons encode sensory information for the execution of behavioural output. Here we show that the temperature-sensing neuron AFD transmits both stimulatory and inhibitory neural signals to a single interneuron AIY. In this circuit, a calcium concentration threshold in AFD acts as a switch for opposing neural signals that direct the opposite behaviours. Remote control of AFD activity, using a light-driven ion pump and channel, reveals that diverse reduction levels of AFD activity can generate warm- or cold-seeking behaviour. Calcium imaging shows that AFD uses either stimulatory or inhibitory neuronal signalling onto AIY, depending on the calcium concentration threshold in AFD. Thus, dual neural regulation in opposite directions is directly coupled to behavioural inversion in the simple neural circuit.

Thermotaxis of C. elegans as a model for temperature perception, neural information processing and neural plasticity

Thermotaxis is a model to elucidate how nervous systems sense and memorize environmental conditions to regulate behavioral strategies in Caenorhabditis elegans. The genetic and neural imaging analyses revealed molecular and cellular bases of this experience-dependent behavior. Surprisingly, thermosensory neurons themselves memorize the sensed temperatures. Recently developed techniques for optical manipulation of neuronal activity have facilitated the revelation that there is a sophisticated information flow between sensory neurons and interneurons. Further studies on thermotaxis will allow us to understand the fundamental logics of neural processing from sensory perceptions to behavioral outputs.

Reconstruction of Spatial Thermal Gradient Encoded in Thermosensory Neuron AFD in Caenorhabditis elegans.

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. SIGNIFICANCE STATEMENT Deciphering 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 property enabled us to reconstruct both neural activity from a temperature stimulus and a spatial thermal environment from neural activity. These results shed light on how a sensory system encodes the environment.

Quantitative behavioral analysis of freely moving C. elegans

P3-f20 Voxel-based morphometry of the relationships between Intelligence Quotient and brain gray matter volume in 156 healthy Japanese children Michiko Asano1, Yasuyuki Taki1, Hiroshi Hashizume1, Yuko Sassa1, Hikaru Takeuchi1, Kohei Asano1, Mijin Lee1, Ryuta Kawashima1,2 1 Division of Developmental Cognitive Neuroscience, IDAC, Tohoku University, Japan; 2 Department of Functional Brain Imaging, IDAC, Tohoku University, Japan

Analysis of glutamate-mediated control of head motor neurons through thermotaxis neural circuit

We examined effects of methionine enkephalin (Met-Enk) on voltage dependent slowly inactivating K+ currents (IKs) in the oculomotor neurons (OMNs) of rats brainstem slices using whole-cell patch clamp techniques. IKs were evoked with depolarizing commands to between −80 and 50 mV with a conditioning pulse to −50 mV in 4-aminopyridine (5 mM)and tetrodotoxin (1 M)-containing Ca2+-free solution and were sensitive to 20 mM tetraethyl ammonium. Reversal potentials of tail currents of IKs were around −100 mV. Met-Enk dissolved in extracellular solution reduced IKs in dose-dependent and reversible manners. Percentage of Met-Enk-induced IKs reduction to control IKs was around 40% (100 M Met-Enk), 30% (75 M), 20% (50 M) and 10% (25 M). The reduction of IKs by Met-Enk was antagonized by opiate receptor antagonist, d-PHE-CYS-TYR-d-TRP-ORN-THR-PEN-THR amide (CTOP, 1 M). We conclude that Met-Enk modulated voltage dependent, TEA-sensitive and slowly inactivating K+ currents in OMNs through activation of opiate receptors.