Stable behavioral and neural responses to thermal stimulation despite large changes in theHydra vulgarisnervous system

Abstract

Nervous systems are remarkable for supporting stable animal behavior despite dramatic changes to neurons' number and connectivity. An ideal model organism to study this phenomenon would have: 1) dynamic neural architecture 2) transgenic reporters of neural activity, 3) a small, transparent body, and 4) well-defined sensory-motor behaviors. While Hydra vulgaris possesses the first three advantages, it currently lacks well-characterized sensory-motor responses. Here, we show the first quantitative measurements of Hydra's behavioral responses to thermal stimulation and associated neural activity.Specifically, we find that Hydra elongate and then contract when heated. This behavior is accompanied by synchronous, periodic activity of neurons in the animal's peduncle. We find that the frequency of these neural oscillations is nearly the same even if the number of neurons change by a factor of two.These observations suggest that Hydra provides a rich model for studying how animals maintain stable sensory-motor responses within dynamic neural circuit architectures.One sentence summary: Here we show that Hydra have a group of thermally responsive neurons that encodes the absolute temperature of a thermal stimulus and that this encoding is independent of the number of neurons in the animal.

In vivofluorescence imaging with a flat, lensless microscope

“…Although movement of the animal can produce some noise in the ∆F/F signal, the deformable Hydra body makes it difficult to generate adaptive ROIs that move with the animal. Nevertheless, the bright synchronous calcium activity in the Hydra peduncle allows for fixed ROIs to effectively capture calcium dynamics 41,45 .…”

Bioelectronics for Millimeter-Sized Model Organisms

“…Bioelectronic platforms combined with calcium imaging can also be applied to other transparent, millimeter-sized animals such as Hydra ( Figure 3C) (Badhiwala et al, 2018;Tzouanas et al, 2019). As is the case for C. elegans, studies of Hydra may help researchers to understand how neural circuits distributed throughout the nervous system regulate simple behaviors such as locomotion and feeding ( Figure 3C).…”

“…However, the unique anatomy of Hydra compared with animals with bilateral symmetry such as C. elegans and zebrafish offer opportunities to study neural circuits in animals with very different neural architectures and body plans. Unlike the nervous systems of C. elegans, Drosophila, and zebrafish that are relatively static and stereotyped, the Hydra nervous system is highly regenerative, variable between animals, and can dynamically change throughout the lifetime of an individual animal (Bode et al, 1973;Gierer et al, 1972;Tzouanas et al, 2019). This characteristic of the nervous system can be used as a powerful tool to understand how the same behavior is regulated when the number of neurons varies by up to an order of magnitude (Tzouanas et al, 2019).…”

“…Unlike the nervous systems of C. elegans, Drosophila, and zebrafish that are relatively static and stereotyped, the Hydra nervous system is highly regenerative, variable between animals, and can dynamically change throughout the lifetime of an individual animal (Bode et al, 1973;Gierer et al, 1972;Tzouanas et al, 2019). This characteristic of the nervous system can be used as a powerful tool to understand how the same behavior is regulated when the number of neurons varies by up to an order of magnitude (Tzouanas et al, 2019). Similarly, these animals can also be used to study neural regeneration following extensive damage (Gierer et al, 1972;Kü cken et al, 2008;Miljkovic-Licina et al, 2007;Technau et al, 2000).…”

“…Using these behaviors, researchers can interrogate fundamental properties of neural circuits such as multisensory integration and sensorimotor transformations (Clark et al, 2013;Ghosh et al, 2017;Kaplan et al, 2018). Among the many behaviors in these animals that enable neural circuit dissection are contractions in the cnidarian Hydra (Dupre and Yuste, 2017;Passano and McCullough, 1964;Tzouanas et al, 2019); thermotaxis, behavioral state transitions, and sleep in C. elegans (Butler et al, 2014;Cho and Sternberg, 2014;Clark et al, 2006;Flavell et al, 2013;Gallagher et al, 2013;Garrity et al, 2010;Hawk et al, 2018;Hedgecock and Russell, 1975;Hill et al, 2014;Kaplan et al, 2019;Li et al, 2014;Raizen et al, 2008); circadian rhythms and social behaviors in Drosophila (Anderson, 2016;Artiushin and Sehgal, 2017;Guo et al, 2018;Kayser and Biron, 2016;Lim et al, 2014;Saigusa et al, 2002;Stockinger et al, 2005); and sensorimotor integration and sleep in zebrafish (Ahrens et al, 2012;Chen et al, 2018;Cong et al, 2017;Gandhi et al, 2015;Haesemeyer et al, 2018;Naumann et al, 2016;Oikonomou and Prober, 2017;Severi et al, 2014;Vladimirov et al, 2018;Zhdanova et al, 2001;Zimmerman et al, 2008). Furthermore, many of these behaviors show a surprising resemblance to mammalian behaviors at the molecu...…”