We review the physiological, molecular, and neural mechanisms of insect color vision. Phylogenetic and molecular analyses reveal that the basic bauplan, UV-blue-green-trichromacy, appears to date back to the Devonian ancestor of all pterygote insects. There are variations on this theme, however. These concern the number of color receptor types, their differential expression across the retina, and their fine tuning along the wavelength scale. In a few cases (but not in many others), these differences can be linked to visual ecology. Other insects have virtually identical sets of color receptors despite strong differences in lifestyle. Instead of the adaptionism that has dominated visual ecology in the past, we propose that chance evolutionary processes, history, and constraints should be considered. In addition to phylogenetic analyses designed to explore these factors, we suggest quantifying variance between individuals and populations and using fitness measurements to test the adaptive value of traits identified in insect color vision systems.

The evolution of color vision in insects.

http://link.springer.com/content/pdf/10.1007/978-3-642-67868-4_4.pdf

Spatial Vision in Arthropods

The visual world offers a variety of information that enables animals to orient themselves to their surroundings. One specific feature of the visual information is the wavelength difference of light emittedfrom light sources or reflectedfrom objects. Under natural conditions, a general difference in the spectral composition of light is based upon the fact that light coming directly from light sources, e.g., the sun, sky, and moon, is characterized by its relatively high content of short wavelength ( 450nm) (Figs. 1). The physical basis of these differences is the preferential absorption by pigment molecules, which—in contrast to atoms and small molecules—have resonances above 300 nm and shift the bulk of the reflected light into the green and orange region of the spectrum. In water, the wavelength range is compressed in the long-wavelength part of the spectrum due to water’s high absorption of red and infrared light (Fig. 1). But in water, too, direct light is relatively richer in shortwave light. Neglecting the finer differences in the spectral content of light, this general distinction between direct and reflected light could be the cue that allows an animal to differentiate such basically different habitats as open spaces, shadowed areas, spaces rich in food, hiding places, etc.

Spectral Sensitivity and Color Vision in Invertebrates

Serial-section electron microscopy has been used to reconstruct the cellular architecture of the posterior nervous system of the nematode Caenorhabditis elegans. Each of 40 neurons in the tail of the adult hermaphrodite can be reproducibly and unambiguously identified by a set of morphological features, including cell body position, fiber geometry and size, and staining properties. A complete list of synapses has been assembled for 2 isogenic animals, and these lists are compared with a third isogenic animal reconstructed by White et al. (1986). The set of neurons and their pattern of synaptic interactions is simple and reproducible. Most of the cells are involved in sensory transduction or in local signal processing to relay signals via a few interneurons to motoneurons and thence to body muscles. Because the tail neurons are well separated and fairly reproducible in position, the hermaphrodite tail lends itself to laser-ablation studies of sensory processing (cf. Chalfie et al., 1985). Most of the synapses in the tail are concentrated in the preanal ganglion. Among the approximately 150 synapses there, about 85% are dyadic chemical synapses. The dyadic synapses are involved in reproducible patterns that have several interesting features. Most neurons synapse onto a few preferred pairs of target cells, in patterns that suggest a combinatorial model of synapse specification that may be open to genetic analysis. Furthermore, most dyadic contacts A----B,C fit a pattern in which the 2 postsynaptic partners are involved elsewhere in unidirectional synapses B----C. Thus, the dyadic synapse may serve to diverge sensory signals into parallel pathways, which then reconverge. This divergence/reconvergence pattern eventually directs processed sensory signals to the ventral cord interneurons PVCL and PVCR. About 80-90% of the synapses fall into repeated classes of synapses. Many of the remaining synapses are widely scattered and irreproducible from one animal to the next. Some of these contacts may be developmental mistakes reflecting a degree of "noise" in synapse specification (Waddington, 1957).

https://www.jneurosci.org/content/jneuro/11/1/1.full.pdf

The posterior nervous system of the nematode Caenorhabditis elegans: serial reconstruction of identified neurons and complete pattern of synaptic interactions

Intracellular recordings were made from the large monopolar cells (LMC's) in the first visual neuropil (lamina) of the flyMusca, whilst applying pharmacological agents from a three-barrelled ionophoretic pipette (Fig. 1). Most of the known neurotransmitter candidates (except the neuropeptides) were tested. The LMC's were most sensitive to histamine, saturating with ionophoretic pulses of less than 2 nC. The responses to histamine were fast hyperpolarizations with maximum amplitudes similar to that of the light-induced response (Fig. 3). Like the light response, the histamine response was associated with a conductance increase (Fig. 5). The histamine responses were not blocked by a synaptic blockade induced by ionophoretic application of cobalt ions (Fig. 6). Several histamine antagonists, and also atropine, were effective at blocking or reducing both the response to histamine and the response to light (Fig. 7). Other transmitter candidates having marked effects on the LMC's were: a) the acidic amino-acids, L-aspartate and L-glutamate, which evoked slower hyperpolarizations that could be blocked by cobalt (Fig. 11); b) GABA, which induced a depolarization associated with an inhibition of the light response (Fig. 9); and c) acetylcholine which also caused a depolarization (Fig. 10). Substances with no obvious effect on the LMC's included serotonin (5-HT),β-alanine, dopamine, octopamine, glycine, taurine and noradrenalin. Together with the evidence of Elias and Evans (1983), which shows the presence, synthesis and inactivation of histamine in the retina and optic lobes of the locust, the data suggest that histamine is a neurotransmitter in insect photoreceptors.

Is histamine a neurotransmitter in insect photoreceptors

Intracellular responses from receptors and postsynaptic units have been recorded in the median ocellus of the dragonfly. The receptors respond to light with a graded, depolarizing potential and a single, tetrodotoxin-sensitive impulse at "on." The postsynaptic units (ocellar nerve dendrites) hyperpolarize during illumination and show a transient, depolarizing response at "off." The light-evoked slow potential responses of the postsynaptic units are not altered by the application of tetrodotoxin to the ocellus. It appears, therefore, that the graded receptor potential, which survives the application of tetrodotoxin, is responsible for mediating synaptic transmission in the ocellus. Comparison of pre- and postsynaptic slow potential activity shows (a) longer latencies in postsynaptic units by 5–20 msec, (b) enhanced photosensitivity in postsynaptic units by 1–2 log units, and (c) more transient responses in postsynaptic units. It is suggested that enhanced photosensitivity of postsynaptic activity is a result of summation of many receptors onto the postsynaptic elements, and that transients in the postsynaptic responses are related to the complex synaptic arrangements in the ocellar plexus to be described in the following paper.

/pdf/neural-organization-of-the-median-ocellus-of-the-dragonfly-i-3jtzytlx9e.pdf

Neural Organization of the Median Ocellus of the Dragonfly I. Intracellular electrical activity

Two types of presumed synaptic contacts have been recognized by electron microscopy in the synaptic plexus of the median ocellus of the dragonfly. The first type is characterized by an electron-opaque, button-like organelle in the presynaptic cytoplasm, surrounded by a cluster of synaptic vesicles. Two postsynaptic elements are associated with these junctions, which we have termed button synapses. The second synaptic type is characterized by a dense cluster of synaptic vesicles adjacent to the presumed presynaptic membrane. One postsynaptic element is observed at these junctions. The overwhelming majority of synapses seen in the plexus are button synapses. They are found most commonly in the receptor cell axons where they synaptically contact ocellar nerve dendrites and adjacent receptor cell axons. Button synapses are also seen in the ocellar nerve dendrites where they appear to make synapses back onto receptor axon terminals as well as onto adjacent ocellar nerve dendrites. Reciprocal and serial synaptic arrangements between receptor cell axon terminals, and between receptor cell axon terminals and ocellar nerve dendrites are occasionally seen. It is suggested that the lateral and feedback synapses in the median ocellus of the dragonfly play a role in enhancing transients in the postsynaptic responses.

/pdf/neural-organization-of-the-median-ocellus-of-the-dragonfly-6ksrlupoyb.pdf

Neural organization of the median ocellus of the dragonfly. II. Synaptic structure.

Spectral sensitivities were recorded intracellulary in median ocelli of Anax junius, Aeschnatuberculifera, and Libellulapulcella. All cells had peak sensitivities at 360 and 500 nm while UV-blue+green cells found only in Anax had a third peak sensitivity at 440 nm. Ratios of UV-to-green sensitivities varied from cell to cell in each ocellus, but no UV-only or green-only cells were recorded. Half of the cells tested had a reverse Purkinje shift: They were more sensitive in the green at low illuminations but more sensitive in the UV at high illuminations; their intensity-response curves at 370 and 520 nm crossed but became parallel for large responses. Wave-lengths 420 nm and shorter elicited a family of low intensity-response curves with one slope; wavelengths 440 nm and longer elicities a family of curves with another slope. Orange-adapting lights selectively adapted sensitivity in the green, but UV-adapting lights had little selective effect. Amounts of log-selective adaptation were proportional to log orange-adapting intensity. It is concluded that two spectral mechanisms can be recorded from each cell, possibly by coupling of UV and green cells or possibly because each cell contains two visual pigments. Selective chromatic adaptations may provide the ocellus with a kind of "authomatic color control," while the reverse Purkinje shift could extend the ocellus' sensitivity to prevailing skylight.

/pdf/action-spectra-and-chromatic-mechanisms-of-cells-in-the-3vgn3a4435.pdf

Action Spectra and Chromatic Mechanisms of Cells in the Median Ocelli of Dragonflies

The intracellular response of the ocellar nerve dendrite, the second order neuron in the retina of the dragonfly ocellus, has been modified by application of various drugs and a model developed to explain certain features of that response. Curare blocked the response completely. Both picrotoxin and bicuculline eliminated the "off" overshoot. Bicuculline also decreased the size of response and the sensitivity. gamma-Aminobutyric acid (GABA), however, increased the size of response. The evidence indicates the possibility that the receptor transmitter is acetylcholine and is inhibitory to the ocellar nerve dendrite whereas the feedback transmitter from the ocellar nerve dendrite may be GABA and is facilitory to receptor transmitter release. The model of synaptic feedback interaction developed to be consistent with these results has certain important features. It suggests that the feedback transmitter is released in the dark to increase input sensitivity from receptors in response to dim light. This implies that the dark potential of the ocellar nerve dendrite may be determined by a dynamic equilibrium established by synaptic interaction between it and the receptor terminals. Such a system is also well suited to signalling phasic information about changes in level of illumination over a wide range of intensities, a characteristic which appears to be a significant feature of the dragonfly median ocellar response.

/pdf/feedback-synaptic-interaction-in-the-dragonfly-ocellar-3ivjmjqxwt.pdf

Feedback synaptic interaction in the dragonfly ocellar retina.

Photographic images of the optokinetic response (OKR) of larval zebrafish permitted the calculation of the amplitude and velocity of the response to gratings of various spatial frequencies rotating at different speeds. At low spatial frequencies, the amplitude of the OKR did not vary significantly for drum speeds ranging from 24 to 108 degrees/sec. Plotting the velocity of the OKR as a function of drum speed gave rise to a bell-shaped curve, with a maximum at about 48 degrees/sec. Interestingly, both eyes exhibited an asymmetric response to the rotating drum, that is, they were more responsive to temporal-to-nasal rotation than to nasal-to-temporal motion. Although this asymmetry persisted over the entire range of drum speeds tested, the situation was reversed when tested with gratings of higher spatial frequency (i.e., the eyes became more responsive to rotation in the nasal-to-temporal direction). The amplitude of the OKR for both eyes exhibited an inverse relation to increasing spatial frequency of the...

Richard L. Chappell

Papers

Neural Organization of the Median Ocellus of the Dragonfly I. Intracellular electrical activity

Neural organization of the median ocellus of the dragonfly. II. Synaptic structure.

Action Spectra and Chromatic Mechanisms of Cells in the Median Ocelli of Dragonflies

Feedback synaptic interaction in the dragonfly ocellar retina.

Directional asymmetries in the optokinetic response of larval zebrafish (Danio rerio).