The Design of Compound Eyes and the Illumination of Natural Habitats
201
eyes are particularly challenged because their eyes are small. They are generally
forced to forsake the well-developed acute zones typical ofbright habitats, in favour
of eye designs that maximize light capture. Superposition eyes, of course, are a popular
option, but there are even apposition eyes that have evolved with extraordinary powers
oflight collection. We have already discussed some of the possible optical strategies
for collecting light by examining Eq. (1): larger apertures, longer photoreceptors
and wider receptive fields all improve sensitivity. So, too, does a higher absorption
coefficient k, and it is interesting to note that in deep-sea animals k is typically 5
times greater than in terrestrial animals (see Warrant and Nilsson 1998). Eyes from
dimmer habitats also typically have much lower F-numbers, a parameter much used
by photographers for comparing the light-gathering power oflenses. The F-number
is simply the focal length divided by the aperture diameter (f !A). A lower F-number
indicates a brighter extended image and a greater sensitivity [sensitivity is inversely
proportional to F-number squared: Eq. (1)].
Even with the most sensitive optical construction possible, a compound eye
may still not collect enough light to meet the visual needs of the animal. In this case,
there is still one more strategy available. This strategy, which resides in the neural
circuits processing the incoming visual signal, involves neural summation oflight in
space and time. When light gets dim, the visual system increases its exposure time,
that is, the time during which a sample of photons is counted. The greater photon
catch that results creates a much more reliable image. Longer exposure times can be
created by slowing down the photoreceptors in dim light (the common method in
nocturnal vertebrates), or by some higher mechanism. This temporal summation,
however, only comes at a price: long exposure times drastically degrade the perception
of fast-moving objects. Too much temporal summation could be disastrous for a
fast-flying nocturnal animal that needs to rapidly judge the presence of approaching
obstacles!
Eyes can also improve image quality by summing photons in space. Instead of
each ommatidia! channel collecting photons in isolation (as in bright light), the
transition to dim light could activate specialized lateral neurons which couple the
channels together into groups (lateral neurons are common in the lamina and medulla,
but as yet it is unknown whether they mediate coupling). In this way each group -
themselves now defining the channels - could collect vastly more photons over a
much wider visual angle, that is, with a greatly enlarged receptive field. Unfortunately,
this improvement in photon catch also comes at a price: this spatial summation results
in a simultaneous and unavoidable loss of spatial resolution. Despite being much
brighter, the image becomes necessarily coarser.
Even though summation compromises spatial and temporal resolution, the gains
in photon catch are so enormous that vision in dim light can be greatly improved. In
fact, the improvements are often so great that some animals are able to see reliably at
light intensities 100 000 times dimmer than those in which they would normally
become blind (Warrant 1999).
How do these strategies for increasing light capture, both optical and neural,
manifest themselves in the compound eyes of animals living in dim habitats?
201
eyes are particularly challenged because their eyes are small. They are generally
forced to forsake the well-developed acute zones typical ofbright habitats, in favour
of eye designs that maximize light capture. Superposition eyes, of course, are a popular
option, but there are even apposition eyes that have evolved with extraordinary powers
oflight collection. We have already discussed some of the possible optical strategies
for collecting light by examining Eq. (1): larger apertures, longer photoreceptors
and wider receptive fields all improve sensitivity. So, too, does a higher absorption
coefficient k, and it is interesting to note that in deep-sea animals k is typically 5
times greater than in terrestrial animals (see Warrant and Nilsson 1998). Eyes from
dimmer habitats also typically have much lower F-numbers, a parameter much used
by photographers for comparing the light-gathering power oflenses. The F-number
is simply the focal length divided by the aperture diameter (f !A). A lower F-number
indicates a brighter extended image and a greater sensitivity [sensitivity is inversely
proportional to F-number squared: Eq. (1)].
Even with the most sensitive optical construction possible, a compound eye
may still not collect enough light to meet the visual needs of the animal. In this case,
there is still one more strategy available. This strategy, which resides in the neural
circuits processing the incoming visual signal, involves neural summation oflight in
space and time. When light gets dim, the visual system increases its exposure time,
that is, the time during which a sample of photons is counted. The greater photon
catch that results creates a much more reliable image. Longer exposure times can be
created by slowing down the photoreceptors in dim light (the common method in
nocturnal vertebrates), or by some higher mechanism. This temporal summation,
however, only comes at a price: long exposure times drastically degrade the perception
of fast-moving objects. Too much temporal summation could be disastrous for a
fast-flying nocturnal animal that needs to rapidly judge the presence of approaching
obstacles!
Eyes can also improve image quality by summing photons in space. Instead of
each ommatidia! channel collecting photons in isolation (as in bright light), the
transition to dim light could activate specialized lateral neurons which couple the
channels together into groups (lateral neurons are common in the lamina and medulla,
but as yet it is unknown whether they mediate coupling). In this way each group -
themselves now defining the channels - could collect vastly more photons over a
much wider visual angle, that is, with a greatly enlarged receptive field. Unfortunately,
this improvement in photon catch also comes at a price: this spatial summation results
in a simultaneous and unavoidable loss of spatial resolution. Despite being much
brighter, the image becomes necessarily coarser.
Even though summation compromises spatial and temporal resolution, the gains
in photon catch are so enormous that vision in dim light can be greatly improved. In
fact, the improvements are often so great that some animals are able to see reliably at
light intensities 100 000 times dimmer than those in which they would normally
become blind (Warrant 1999).
How do these strategies for increasing light capture, both optical and neural,
manifest themselves in the compound eyes of animals living in dim habitats?