Processing of spectral information in the dragonfly lamina
Date
1994
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Yang, En-Cheng
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In this thesis, intracellular recordings were made from the photoreceptors and large monopolar cells (LMCs) of the dragonfly, Hemicordulia tau, to study the spectral information processing in the early vision of the insect compound eye. Photoreceptors recorded from the ventral region of the compound eye could be divided into five groups (360 nm, 420 nm, 460 nm, 530 nm and 590 nm) according to their peak spectral sensitivities. Compared to the previous study by S. Laughlin in 1974, where only three spectral classes of photoreceptors were reported, the 420 nm and 600 nm classes of photoreceptors are a new discovery.
The spectral sensitivities of five types of LMC (cell type 1-5) were also recorded. Cell type 1 exhibits a broad spectral sensitivity function with maximal sensitivity between 480 nm and 510 nm. The spectral sensitivity of cell type 2 has two peaks, one in the region between 500 nm and 550 nm and another in the UV region. The spectral sensitivities of cell types 3 and 4 are similar to the 420 nm and 530 nm photoreceptors, respectively. The main sensitivity peak of cell type 4 is in the 500-550 nm region. The spectral sensitivity of cell type 5 is also similar to 530 nm photoreceptor, but the main sensitivity peak is at 500 nm. When dark-adapted, the monopolar cells had peak spectral sensitivities that were similar to single photoreceptors, or appeared to pool the outputs of receptors with different spectral sensitivities. In some cases, spectral sensitivity changed markedly upon light adaptation. For example, when cell type 2 was light-adapted by 550 nm, its sensitivity to UV light was suppressed. On the other hand, when cell type 5 was light-adapted by 550 nm, the absolute sensitivity to 520 nm was increased, though the spectral sensitivity remained the same as in the dark-adapted state. These effects cannot be explained by selective spectral adaptation. Rather, they suggest that this cell type receives synaptic input from more than one spectral class of photoreceptor, and that adaptation alters the computation of this input in unexpected ways. A control experiment on fly LMCs, which are known to receive input from a single spectral class of photoreceptors, showed no spectral sensitivity change in the light adapted state, as expected. These results suggest that the changes of spectral sensitivity in the light-adapted lamina monopolar cells of the dragonfly are mediated by the interaction of different spectral types of photoreceptors. Previous studies in fly lamina (Laughlin, 1974b; Srinivasan et al., 1982; Laughlin and Osorio, 1989) indicated that lateral inhibition affects the spatial and temporal properties of lamina cells. Because the lateral inhibition of the LMC could be mediated by extracellular photocurrents or particular synaptic inputs (Laughlin, 1974a,b; Shaw,1975), I attempted to identify the origin of the lateral inputs by measuring their spectral sensitivities as well as looking at their spatio-temporal properties with white-noise stimulation. The spectral sensitivities of the inhibitory inputs recorded from two types of UV-sensitive LMCs (cell types 2 and 4) in the dark-adapted state were different from their spectral sensitivities measured from the hyperpolarizing centre in the dark adapted state, but similar to those on 550 nm light adaptation. That is, the surround spectral sensitivity of cell type 2 has a single peak in 500-520 nm region, while cell type
4 has its sensitivity peak at 340-360 nm. These results suggest that a synaptic lateral inhibitory input to the hyperpolarizing centre of the LMC receptive field is provided from neighbouring lamina cartridges. Experiments with white-noise stimulation were carried out to determine the characteristics of the inhibition and the shape of its receptive field. Two spatial configurations Were used for the white-noise experiments: one having the spatial form of a checkerboard and the other a spot with a surrounding annuals. Analysis of the kernels obtained from checkboard white-noise experiments reveals that the inhibitory signal has a longer latency than that from the excitatory centre. The spatio-temporal receptive fields of the dragonfly LMCs show that the shapes of the inhibitory fields are diverse, but most of them are hi-lobed. None of the dragonfly LMCs has a receptive field with concentric centre-surround configuration. The nonlinear properties of the LMCs were examined using spot-annulus white-noise stimulus. The reversed polarity found between the second-order kernels of the hyperpolarizing centre and depolarising surround indicate an inverted, nonlinear signal contributed by the surrounding cartridges. These observations are consistent with the presence of synaptic lateral inhibition, in addition to the electrical field inhibition that has been postulated as the primary mechanism for generating the inhibitory fields of lamina neurons in the insect eye (Laughlin, 1974b; Shaw, 1975). Since the lateral inhibition provides both spatial and spectral antagonism to the LMCs, it is evident that colour opponency plays an important role in the processing of spectral information in the dragonfly lamina.
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