Colour vision in mantis shrimps: understanding one of the most complex visual systems in the world

Thoen, Hanne (2015). Colour vision in mantis shrimps: understanding one of the most complex visual systems in the world PhD Thesis, Queensland Brain Institute, The University of Queensland. doi:10.14264/uql.2015.409

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Author Thoen, Hanne
Thesis Title Colour vision in mantis shrimps: understanding one of the most complex visual systems in the world
School, Centre or Institute Queensland Brain Institute
Institution The University of Queensland
DOI 10.14264/uql.2015.409
Publication date 2015-03-13
Thesis type PhD Thesis
Open Access Status Other
Supervisor Justin Marshall
Martin How
Total pages 156
Language eng
Subjects 060805 Animal Neurobiology
060201 Behavioural Ecology
060602 Animal Physiology - Cell
Formatted abstract
Stomatopods (commonly known as mantis shrimps) have one of the most complex visual systems in the animal kingdom with up to 20 different photoreceptor types and the ability to see both linear and circular polarized light. The eye of a stomatopod is divided into three different parts; a dorsal and a ventral hemisphere divided up by 6 distinct rows of specialised ommatidia (visual units) termed the midband. The midband contains a complex array of up to 12 spectral receptors with maximum sensitivities ranging from the ultraviolet (UV) to the far-red (300-700 nm), in addition to achromatic receptors of which several are sensitive to different forms of polarized light. The abundance of spectral receptors has puzzled researchers, as it seemed excessive even for an animal living in a spectrally rich environment such as the coral reef. Furthermore, theoretical analyses suggest that there is really no need to have more than 4-7 receptors to have satisfactory colour vision in the 300-400 nm spectral range. Our increasing knowledge of polarization sensitivity is rapidly expanding the theme of photoreceptor proliferation with up to six channels of polarization information from a combination of midband and hemisphere receptors.

The aim of this thesis was to investigate how stomatopods process and analyse chromatic and polarization information using a complementary approach of behavioural, electrophysiological and neuroanatomical techniques. A comparison of spectral sensitivities across species in the superfamily Gonodactyloidea was carried out in Chapter 2. This study showed that their spectral sensitivities remain very similar between species, with narrow, steeply shaped sensitivity curves spread evenly throughout the spectrum, suggesting there is a benefit of having uniform sampling of all wavelengths. Behavioural experiments were performed to test stomatopod spectral discrimination in Chapter 3, and this was found to be surprisingly poor, both compared to other animals and to theoretical modelling. To investigate if the poor discrimination was due to the spectral shape of the stimuli, more natural-shaped stimuli (with step-shaped spectra instead of the conventional peak-shaped spectra) were tested in similar experiments (Chapter 4). However, these experiments yielded similar results to the ones obtained in Chapter 3. The electrophysiological and behavioural results suggest that the stomatopod visual system may use a simpler, serial processing system unlike the "conventional" opponency system known from other animals and may be the reason for why the spectral and polarization space must be covered by several channels.

While such as system may appear exceptional, there are similarities between this system and they way primates process colour, only at different steps in the processing pathway (Chapter 5). Using an interval-decoding scheme coupled with the narrow, binned spectral sensitivities of stomatopods could allow quick and precise colour judgements but at the cost of very fine discrimination.

As very little was known about the neural architecture of the stomatopods visual system, and to investigate possible answers to questions posed in Chapter 2-5, a range of methods was employed to examine the various neuronal structures. These included: immunohistochemistry experiments and 3D-reconstructions to visualise the gross morphology of the optic lobes, Bodian staining and fluorescent tracer injections to investigate the neuronal pathways, and Golgi impregnations to identify single neuronal types (Chapter 6). First, observations from previous studies were confirmed, in that the midband information pathway remains visible throughout the three first optic lobes as a distinct swelling (Kleinlogel et al., 2003). Chapter 6.2 describes the cell types found in the first optic neuropil, the lamina, where despite size and shape differences between some cells, no clear specializations were observed in the midband region compared to the hemispheral regions of the lamina.

The stomatopod medulla was described in Chapter 6.3 and was shown to be clearly stratified having at least 12 main layers, with the midband pathway distinctly visible as a swelling on the distal side of the medulla. The chromatic information appears to be integrated with the achromatic information in the lobula (the third optic lobe, Chapter 6.4) with lateral collaterals forming in the midband pathway and projecting into the hemispheral regions of the lobula. Further projections from the lobula terminate in optic glomeruli in the lateral protocerebrum, which may be involved in refining and sharpening the signals from the lobula columnar neurons. Finally, the stomatopod central complex in the cephalic brain was described in Chapter 6.5, revealing that stomatopods have a central complex more similar to that of an insect than to other crustaceans, possibly shedding new light of to the evolutionary relationship between crustaceans and insects.

Overall, this study has given new insights into how stomatopods process chromatic and polarization information. It has revealed a system that at the photoreceptor level appears very complex, but that not necessarily requires high levels of complex processing. These findings may provide inspiration to the development of new optic and camera technologies, and propose a sparse signal-processing scheme, which could provide useful in artificial imaging technologies that require fast and low-power processing speeds.  
Keyword Stomatopod
Opponent processing
Optic pathways

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Created: Sat, 07 Mar 2015, 02:19:43 EST by Hanne Thoen on behalf of Scholarly Communication and Digitisation Service