Insights into light sensing, eye evolution and neural regeneration


21 Aug 2017

Insights into light sensing, eye evolution and neural regeneration

 

By Dr Dasaradhi Palakodeti, Intermediate Fellow 2010

Institute for Stem Cell Biology and Regenerative Medicine, Bangalore

 

The coordinated interplay between the brain and the eye has fascinated biologists for a long time. After all, that is the basis of ‘vision’ as we know it. But what has been a bone of contention between the creationists and the evolutionary biologists, is the origin of this network. As famously stated by Theodosius Dobzhansky, “Nothing in biology makes sense except in the light of evolution”. To our knowledge, planarians are among the earliest organisms that have developed a ‘brain’ and ‘eye’ in the evolutionary tree. They are flatworms that have a rich neural architecture with a cerebral eye, a bi-lobed brain (dorsal ganglion) and a ‘peripheral’ nervous system that includes a ventral nerve cord. Added to that is a unique capacity for extensive regeneration (including the brain and the eyes!) upon amputation, that makes them an excellent model to study the function of the eye and the brain. So, we decided to understand the eye-brain conundrum in the planarian, Schmidtea mediterranea.

Using Schmidtea mediterranea as a model system, we now have clearer insights about how light is sensed in nature. We have also been able to link these novel aspects of light sensing to regeneration and functional recovery. Contrary to prior expectations, we observed that planarians could decipher minute differences in the input light, despite possessing a very simple eye architecture. Using detailed light sensing studies and fluorescence imaging, we show that the ‘color-blind’ worms could ‘discriminate’ between light stimuli of different wavelengths (‘colors’) with maximum efficiency. They cannot truly ‘perceive’ different wavelengths but use a trick. They convert light wavelength differences into a light ‘intensity’ changes, allowing them to ‘sense’ small wavelength differences. In simpler terms, they turn spectral information (colors) into very refined, shades of gray. Our work thus demonstrates that the planarian cerebral eye and nervous system has the ability to accomplish fairly sophisticated ‘comparative processing’, that enables them to sense these small differences and switch their behavior accordingly, which we think is truly remarkable. This is an exciting finding and has implications for eye-brain evolution. 

We are interested in understanding the neural network between the eye and the brain that allows the organism to exhibit such complex behavior. Interestingly, this is where regeneration comes in handy! If we cut away the heads of the worms, they should not be able to sense light. But these are planarians after all, so over time they will regenerate their eyes and their brain!

This is where this story gets another twist. These worms also seem to sense light without eyes. If we shine even tiny amounts of long UV light, headless worms start moving like intact worms, and show an escape response! This reflex-like response is quite different from the eye-brain sensing. Also, during regeneration, if we time it just right, we find worms that can sense light (they are not blind) but cannot compare small differences! Then as their eyes and brain connections strengthen, they build the right neural connections and their abilities gradually recover!! In essence, we can separate this ability of the neural network to ‘process’ or ‘compute’ from simple/crude light sensing. Also, we can watch the recovery of ‘comparative processing’, which is quite unique!

So we have two amazing but very different light sensing networks in one organism; allowing us to do really unique experiments. We were even able to challenge the worms with choices and ask which neural network would be stronger, the reflex-like whole body network or the brain based network?

In this paper we show that in intact worms, the eye-brain response can override the whole body response. This was quite striking and is reminiscent of hierarchies in neural networks in more complex animals and mammals. However, studying this extra-ocular (eye-independent) light sensing during eye-brain regeneration show that these hierarchies are very dynamic. During regeneration, there are time-points where the whole-body response is actually stronger, not yet under control of the newly forming eye and brain. Then in a clear, sharp switch, the eye-brain network reclaims its dominance! We believe that this switching depends on how the regenerating neural networks re-wire and connect to each other.

We are currently looking at molecular players that are critical for regulating eye and brain regeneration. Our new findings allow us to ask how is a simple light sensing eye and brain network able to ‘compute’ and compare small differences? This will help regeneration biology (eye and brain) as well as help our understanding of how vision and neural processing evolved.

The exciting thing is: we now have a method to visualize this connectivity and competition between the two very different neural networks – all in the same animal. This opens a new area of research where we can address the molecular and structural mechanisms underlying neural regeneration and function.

In summary, for these worms, light matters! They have evolved the ability to process light in multiple different yet sophisticated ways using seemingly simple sensing apparatus, as they must have adapted to their complex natural habitats. Overall our work illustrates how curiosity driven, highly collaborative research not only leads to new discoveries but can also impact problems related to neural regeneration that have tremendous biomedical relevance!

This is a collaborative work between our group and Dr. Akash Gulyani's at Institute for Stem Cell Biology and Regenerative Medicine, Bangalore.

 

Hierarchies in light sensing and dynamic interactions between ocular and extraocular sensory networks in a flatworm. Nishan Shettigar, Asawari Joshi, Rimple Dalmeida, Rohini Gopalkrishna, Anirudh Chakravarthy, Siddharth Patnaik, Manoj Mathew, Dasaradhi Palakodeti* and Akash Gulyani*. Science Advances. July 2017