A Brain-wide Circuit Model of Heat-Evoked Swimming Behavior in Larval Zebrafish

• Published in: Neuron (Cambridge, Mass.) Mass.), 2018-05, Vol.98 (4), p.817-831.e6
• Main Authors: Haesemeyer, Martin, Robson, Drew N., Li, Jennifer M., Schier, Alexander F., Engert, Florian
• Format: Article
• Language: English
• Subjects: Algorithms; Animals; Behavior; Behavior, Animal; Brain - diagnostic imaging; Brain - metabolism; Brain - physiology; Brain research; Calcium imaging; Calcium Signaling; Calcium signalling; circuit model; Cold; computation; Computational neuroscience; Danio rerio; Drosophila; Functional Neuroimaging; Ganglia; Heat; Heat stimuli; Hindbrain; Hot Temperature; Hypothesis testing; Information processing; Insects; Larva; modeling; Neural Networks, Computer; Neural Pathways; Neuroimaging; Neurons; Neurons - metabolism; Neurons - physiology; representation; Rhombencephalon - diagnostic imaging; Rhombencephalon - metabolism; Rhombencephalon - physiology; Sensorimotor integration; Sensory integration; Sensory neurons; Software; Spinal cord; Swimming; Swimming behavior; Temperature effects; thermosensation; Thermosensing - physiology; Trigeminal ganglion; Trigeminal Ganglion - diagnostic imaging; Trigeminal Ganglion - metabolism; Trigeminal Ganglion - physiology; Zebrafish
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2018.04.013

Thermosensation provides crucial information, but how temperature representation is transformed from sensation to behavior is poorly understood. Here, we report a preparation that allows control of heat delivery to zebrafish larvae while monitoring motor output and imaging whole-brain calcium signals, thereby uncovering algorithmic and computational rules that couple dynamics of heat modulation, neural activity and swimming behavior. This approach identifies a critical step in the transformation of temperature representation between the sensory trigeminal ganglia and the hindbrain: A simple sustained trigeminal stimulus representation is transformed into a representation of absolute temperature as well as temperature changes in the hindbrain that explains the observed motor output. An activity constrained dynamic circuit model captures the most prominent aspects of these sensori-motor transformations and predicts both behavior and neural activity in response to novel heat stimuli. These findings provide the first algorithmic description of heat processing from sensory input to behavioral output. [Display omitted] •Temperature stimuli were combined with functional imaging and behavior recording•Heat- and motor-encoding neurons were mapped throughout the larval zebrafish brain•A critical transformation in heat representation was identified in the hindbrain•A dynamic circuit model captures and quantifies the sensori-motor transformations Haesemeyer et al. combine calcium imaging with behavioral recording and circuit modeling to reveal how temperature information is encoded and transformed in a vertebrate brain to generate behavior using a dynamic modeling strategy suited to capture temporal transformations in activity.