Whole-body imaging of neural and muscle activity during behavior inHydra: bidirectional effects of osmolarity on contraction bursts

Abstract

The neural code relates the activity of the nervous system to the activity of the muscles to the generation of behavior. To decipher it, it would be ideal to comprehensively measure the activity of the entire nervous system and musculature in a behaving animal. As a step in this direction, we used the cnidarian Hydra vulgaris to explore how physiological and environmental conditions alter the activity of the entire neural and muscle tissue and affect behavior. We used whole-body calcium imaging of neurons and muscle cells and studied the effect of temperature, media osmolarity, nutritional state and body size on body contractions.In mounted Hydra, changes in temperature, nutrition or body size did not have a major effect on neural or muscle activity, or on behavior. But changes in media osmolarity altered body contractions, increasing them in hipo-osmolar media solutions and decreasing them in hyperosmolar media. Similar effects were seen in ectodermal, but not in endodermal muscle.Osmolarity also bidirectionally changed the activity of contraction bursts neurons, but not of rhythmic potential neurons.These findings show osmolarity-dependent changes in neuronal activity, muscle activity, and contractions, consistent with the hypothesis that contraction burst neurons respond to media osmolarity, activating ectodermal muscle to generate contraction bursts. This dedicated circuit could serve as an excretory system to prevent osmotic injury. This work demonstrates the feasibility of studying the entire neuronal and muscle activity of behaving animals. Significance StatementWe imaged whole-body muscle and neuronal activity in Hydra in response to different physiological and environmental conditions. Osmolarity bidirectionally altered Hydra contractile behavior. These changes were accompanied by corresponding changes in the activity of one neuronal circuit and one set of muscles. This work is a step toward comprehensive deciphering of the mechanisms of animal behavior by measuring the activity of all neurons and muscle cells.

Large-scale neural recordings call for new insights to link brain and behavior

“…In smaller, transparent animals such as larval zebrafish, C. elegans, and hydra, activity of the majority of neurons can be imaged simultaneously at cellular resolution in the fully intact animal (Ahrens et al, 2013;Schrödel et al, 2013;Yamamoto and Yuste, 2019)(see Box). During unrestrained animal movements, fast-tracking microscopes move to keep up with the animal as it swims or crawls (Nguyen et al, 2016;Venkatachalam et al, 2016;Cong et al, 2017;Kim et al, 2017b;Symvoulidis et al, 2017) (Figure 1a).…”

“…The answer to this question depends heavily on the size and physical properties of the brain in question. Simultaneous whole-brain measurements of single-neuron activity have been acquired in small, transparent animals, notably the worm C. elegans (Schrödel et al, 2013), larval zebrafish (Ahrens et al, 2013), hydra (Yamamoto and Yuste, 2019) and perhaps soon in Drosophila (Mann et al, 2017). In mammals, recording electrophysiological activity across all cortical neurons is possible in principle (Kleinfeld et al, 2019), especially when allowing for recording techniques based on novel physical principles (Marblestone et al, 2013).…”

From neuron to muscle to movement: a complete biomechanical model ofHydracontractile behaviors

“…We assume that CBs are initiated by repeated stimulation of the fast pathway in a ring of muscle cells at the peduncle. What causes the CB nerve net to fire is still not known, although it is influenced by conditions such as osmolarity (Yamamoto and Yuste, 2019) , microbes (Murillo-Rincon et al, 2017) and temperature (Tzouanas et al, 2019) . While the CB nerve net is distributed, it has a high density of neurons at the peduncle and we assume these to be the primarysource of activation.…”

“…The rules that govern the generation of the neural activity are still an open question. Recent experiments have shown that temperature (Tzouanas et al, 2019) and osmolarity (Yamamoto and Yuste, 2019) can influence the CB firing rate in Hydra. Neural activity is likely to be influenced by the behavior or the state of the animal through mechanosensation and other sensory inputs.…”