Sensory Systems/Jellyfish

Introduction
Nearly all living organisms are capable of light sensing, that is, responding to electromagnetic radiation in the range of 300-800 nm. Studying visual systems is fascinating from the evolutionary point of view because animals which are very distant from each other on the tree of life seem to have developed surprisingly similar, sometimes very complex machinery that allows them to sense light. Of particular notice is the visual system of the box jellyfish (Class Cubozoa, Phylum Cnidaria) (Figure 1): it is the most elaborate cnidarian visual system. The eyes of these beautiful aquatic animals are very similar to our own! The exceptional vision of the members of the Cubozoa class (the smallest class in the phylum Cnidaria) was detected when it was noticed that they demonstrate unexpectedly complex swimming behaviours: they can move very fast in specific direction and avoid dark areas and obstacles.



There is a number of experimental procedures that allow scientists to study how box jellyfish see. For example, by controlling lighting conditions in experimental chambers where animals are tethered one can observe changes in pulse frequency, contractions and structural asymmetry of the bell of the jellyfish which would translate into avoidance and approach swimming behaviours in free animals. In the past decades the nervous system of the box jellyfish including visual system has been studied from anatomical, cellular, molecular and genetic perspectives but the knowledge of the elaborate eyes of these creatures is still incomplete.

Anatomy
Box jellyfish has its name for the cube-like shape of its bell, which is about 10 mm in diameter in adult animals. On each side of the bell are situated the four rhopalia – sensory structures that accommodate in total 24 eyes of various types. Such positioning of the visual organs allows Cubomedusae to have a nearly 360-degree view of the surrounding! Remarkably, their eyes do not look outside but inside of the medusa (i.e. at each other!) but thanks to the transparency of the bell can still see in all directions. Jellyfish lack the ability to control eye position with muscles, so rhopalia maintain the same natural orientation independent of the orientation of the bell with the help of the crystal structure in the bottom called statolith that acts as a weight and the flexible stalk on top that connects them to the bell. The six eyes in the rhopalia are of four different morphological types (Figure 2): upper and lower complex lens human-type eyes (ULE and LLE) at the vertical midline, and paired simple eyes with light-sensitive pigment only on each side, called pit and slit eyes (PE and SE).

Although cnidarians are radially symmetrical organisms, the nervous system inside their rhopalia is bilaterally symmetrical, except the midline positioning of the lens eyes. The stalk with a rhopalial nerve inside serves as connection between a rhopalium and the ring nerve at the bell margin which in turn is connected to the nerve net, forming together the complete nervous system of the box jellyfish.



Both neuronal and non-neuronal cells have been described in the rhopalia, forming different cell populations.The neuronal cells cluster in two bilaterally symmetrical groups connected to each other and to pit and slit eyes with fiber pathways. All in all, there are over 1000 neuronal cells in the rhopalium, including: Non-neuronal cells include ciliated photoreceptor cells responsible for the initial light sensing, balloon cells of unidentified function and posterior cell sheet - the largest cell population of undifferentiated cells which are possibly associated with the nervous system.
 * retina-associated neurons linked to lens eyes
 * flank neurons
 * giant neurons

Lens eyes
The lens eyes of box jellyfish are astonishingly similar to our own due to the presence of the camera with vitreous body separating the lens and the retina (hence the name “camera eye”). The lens eyes are known to have poor spatial resolution because the retina is very close to the lens separated only by thin vitreous space (around 8 μm in the lower lens eye, absent in upper lens eyes) with focal length of the lens falling far beyond the retina (between 400-600 μm). In humans, by contrast, the size of the camera is about 23 mm. Using a special procedure during which an electrode placed in the eye records activity of cells there in response to various visual stimuli called electroretinography, the temporal properties of the upper and lower lens eyes have also been determined. Both eye types have low temporal resolution but their response patterns differ suggesting that they are utilized for different visual tasks. For example, the maximum frequencies that can be resolved from the electroretinograms (also called flicker fusion frequencies) by the upper and lower lens eyes were reported to be 10 and 8 Hz, respectively. Apart from that, the two lens eyes have different visual fields covering different areas of the surroundings. Overall, it seems plausible that eyes of the box jellyfish are fine tuned to perform specific tasks which in turn allows filtering of the visual stimuli already in the rhopalia.

Do box jellyfish have colour vision?
A curious question is whether members of the Cubomedusae order have colour vision like more advanced vertebrate organisms including us do. There are two types of photoreceptors in the animal kingdom: ciliary, usually present in vertebrates, and rhabdomeric, found in invertebrates. Interestingly, box jellyfish possess vertebrate-like ciliary photoreceptors. Although both types rely on the same chemical conversion of the retinal molecule upon exposure to light (i.e. bleaching), they differ in the mechanism, structure, origin and molecular pathways. The type of receptors in the retinas of both upper and lower lens eyes are normally sensitive to the blue-green light with peak absorbance between 465-508 nm depending on a species. The available data to date therefore suggests that box jellyfish might be sensitive to green light although experiments in green colour-guided obstacle avoidance produced inconclusive results. Colour vision would be a useful adaptation for these animals living in shallow water with lots of flickering light at the surface ripples to discern the luminance (i.e. brightness, intensity) noise from relevant visual stimuli, as colour vision is less sensitive to luminance fluctuations.

Visual processing and control of swimming behaviour
To date, only the importance of the lower lens eyes for the control of swimming behaviour has been experimentally established, including their role in bell contraction rates which modulate the speed of the moving animal. Notably, the optical power of lens eyes varies between species of the Cubomedusae introducing further variability. The role of slit and pit eyes in pacemaker activity (pulsating movement of the bell) and control of swimming direction remains somewhat unclear and can be elucidated in future experiments where specific eye types are selectively made non-functional.



It is also not entirely clear how integration of the visual input occurs in the nervous system of the box jellyfish. Response to visual stimulus was detected both in the stalk (an extension of the nerve ring) as well as the nervous system of the rhopalium itself. The association of specific neuronal cells with certain eye types within the rhopalia signifies that some but not all information processing and integration occurs within these structures. Perhaps the speed of swimming which depends on the rate and strength of the contractions of the body and tentacles of the jellyfish is controlled by the pacemaker activity of a distinct neuronal population that is responsible for higher-order processing and integration of the visual information. Flank and giant neurons might serve this function. The fine steering might in turn be controlled through independent signalling and asymmetrical contraction of the different sides of the bell.

Evolutionary perspective
Genetically, the visual system of the box jellyfish also appears to be more closely related to that of vertebrates rather than invertebrates, because they share several critical components of the molecular pathways underlying light sensing (for example, phosphodiesterases needed for phototransduction and protective pigment-producing machinery in the retina). The bilateral organisation of the rhopalium nervous system (with the exception of the retina associated neurons) in the otherwise radially symmetrical jellyfish could be the evidence that cnidarians evolved from a bilaterally symmetrical ancestor, but the use of the ciliary photoreceptors and melanogenic pathway by both box jellyfish and vertebrates could mean either common ancestry or independent parallel evolution. Further investigation of the extraordinary visual system of the box jellyfish would therefore be helpful in solving the riddle on the evolutionary origin of the advanced camera eyes.