Neural connections behind the complex retina of the stomatopod (Mantis shrimp)

Kleinlogel, Sonja (2004). Neural connections behind the complex retina of the stomatopod (Mantis shrimp) PhD Thesis, School of Biomedical Sciences, The University of Queensland.

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Author Kleinlogel, Sonja
Thesis Title Neural connections behind the complex retina of the stomatopod (Mantis shrimp)
School, Centre or Institute School of Biomedical Sciences
Institution The University of Queensland
Publication date 2004
Thesis type PhD Thesis
Supervisor Assoc. Prof. N. Justin Marshall
Assoc. Prof. Shaun P. Collin
Total pages 246
Language eng
Subjects 270502 Neurobiology
Formatted abstract

This study is the first to examine the visual neuroarchitecture of gonodactyloid stomatopod species native to Australia. It also presents the first electrophysiological measurements of polarization sensitivity of stomatopod photoreceptors.      

Gonodactyloids possess regionally specialised apposition compound eyes. The tripartite eyes consist of a dorsal and a ventral hemisphere bisected by a band, termed the midband. This band consists of six rows of anatomically and functionally specialised ommatidia. The hemispheric retinae are typical of other crustacean eyes and whilst they mediate spatial vision, the mid-band is concerned with colour and polarization vision and contains fourteen spectral and four e-vector sensitivities.

Although much is known about the intriguing retinal capabilities of stomatopods, almost nothing is known about how this information is processed. Therefore, the aim of this study was to analyse the neuroarchitecture of the eye, in particular the photoreceptor wiring and termination pattern. This study reveals how the multiple channels of information supplied by the retina are communicated to deeper levels of the brain and provides a basis for future functional investigations on the coding mechanisms underlying peripheral visual processing.       

After presenting an introduction to the visual world of stomatopods and the methodology utilised, Chapter 3 examines the gross anatomy of the first three visual neuropils; the lamina, the medulla externa and the medulla interna. All three neuropils have an accessory lobe, which receives axonal projections exclusively from the mid-band. Spatial, colour and polarization information is divided into three parallel data streams from the retina to, at least, the medulla externa.    

Serial light- and electron microscopy was used to trace individual photoreceptor axons from the retina to the lamina (Chapter 4). The retina-to-lamina photoreceptor projection is retinotopic, therefore preserving spatial information. Each lamina cartridge consists of two lamina strata, separating the two channels of colour and polarization within each ommatidium. The projection and lamina termination pattern is identical throughout the eye, regardless of the retinal partitioning. This suggests colour and polarization opponency.       

Chapter 5 investigates the termination pattern of short visual fibres in more detail. Photoreceptors form triad synapses onto the first order interneurons, the monopolar cells, using histamine as their neurotransmitter. Terminals of the inner lamina stratum are dye-coupled due to their close proximity.        

Photoreceptor spectral sensitivity measurements are presented in Chapter 6. They confirm the large number of ultraviolet sensitivities in the retinae of gonodactyloid stomatopods and reveal double-peaked spectral sensitivity curves for retinula cells 1 to 7 (R1-7). The secondary maximum lies in the ultraviolet and suggests a synaptic input from the ultraviolet-sensitive 8th retinula cell (R8).       

The projection and termination pattern of the long visual fibre R8 is presented in Chapter 7. The R8 cells terminate superficially within the second optic neuropil, the medulla externa. R8 cells from neighbouring mid-band rows are dye-coupled and could potentially form additional colour and polarization opponency channels in the ultraviolet. It is proposed that the colour vision system of gonodactyloid stomatopods consists of six dichromatic colour channels, four in the visible and two in the ultraviolet part of the spectrum. Furthermore, R8 cells of the hemispheres and mid-band rows 1-4, but not of mid-band rows 5 and 6, form contacts with short visual fibre terminals in the lamina. This suggests that the R8 cells of mid-band rows 5 and 6 form a separate neural pathway from R1-7 cells.        

Chapter 8 examines aspects of polarization vision. A novel polarization signal and first electrophysiological polarization sensitivity measurements of photoreceptors are presented. It is suggested that the polarization vision system of stomatopods is designed for two-dimensional 'static' polarization vision in two spectral bands. A third, temporal dimension may be added to the systems by slow scanning eye movements.        

Chapter 9 is a general discussion. The findings of this study support the suggestion from previous behavioural observations that signal recognition is a principal task of stomatopod eyes. It is postulated that the colour and polarization vision systems of stomatopods have co-evolved with colour and polarized light reflecting body markings. During phylogenetic development the neural wiring beneath the retina remained unchanged and instead, a complex retina evolved that is able to collect multiple visual cues simultaneously and already sorts the information into parallel data streams. The eyestalk neuropils and the brain are thus left with the relatively simple task of encoding the already disentangled visual information. 

Keyword Stomatopoda
Retina -- Innervation

Document type: Thesis
Collection: UQ Theses (RHD) - UQ staff and students only
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