The Metabolic Cost of Information- a Fundamental Factor in Visual Ecology
181
previously observed (Autrum 1958), it is the slower-flying insects that have
slower responses.
Fast responses are metabolically expensive because they require a membrane
with a short time constant. The membranes of fast photoreceptors contain delayed
rectifier potassium conductances that adapt the membrane for a fast response by
lowering the membrane resistance, and hence time constant. This low resistance
draws large currents. The membranes of slow photoreceptors are specialized to
reduce current (Weckstrom andLaughlin 1995). Unlike the delayed rectifiers of
fast cells, the slow cell potassium conductance responds transiently because it
inactivates. Inactivation reduces current flow and, by increasing resistance,
increases the membrane time constant. The longer time constant smooths out rapid
fluctuations in membrane voltage, but unlike fast cells, where this smoothing
would destroy fast signals, in slow cells this smoothing is advantageous (Laughlin
1996). In an insect that moves slowly and views the world through poor optics, a
rapid change in receptor response is almost certainly noise.
Fast and slow photoreceptors exemplify visual ecology in the time domain. The
dynamics of vision are matched to the dynamics of natural signals, as dictated by
life style and habitat, to strike appropriate balances between costs and benefits.
Outside of insects, comparative data is conspicuously absent, but the matching of
dynamics to life style might be widespread. Birds have higher flicker fusion
frequencies than other vertebrates (pigeon 140 Hz; chicken I 00 Hz - cited in
Laughlin and Weckstrom 1993) and there are suggestive differences among fish
(Lythgoe 1979). Matching occurs at higher levels of visual processing. The
motion sensitive neurons of hovering insects (e.g. hawkmoths and hoverflies),
respond better at lower velocities than those of insects whose flight is less well
stabilised (e.g. butterflies, blowflies and bees). Sensitivity to lower velocities is
achieved with longer time delays in motion detectors (O'Carroll et al. 1997).
Warming the retina could match response dynamics to visual ecology (Block
1986). Fast moving fish (swordfish, tuna) heat their retinas and fast moving
insects (dragonflies, honeybees) heat their heads (Heinrich 1993). Heating
improves the temporal resolving power ofphotoreceptors (Tatler et al. 2000).
The significance of economizing on photoreceptor energy usage is emphasized
by the degree to which photoreceptor response dynamics are fme-tuned.
Adaptations of response dynamics occur among photoreceptors of the same
spectral and morphological class, within one species. There are examples of a
sexual dimorphism of photoreceptor voltage response. In bibionids and in the
housefly Musca, the male has an eye region that is enlarged to detect, follow,
intercept and hopefully mate with females (Land 1997). The photoreceptors in this
male region have faster responses which, when combined with their better optics,
improves the resolution of small and rapidly moving targets (Laughlin and
Weckstrom 1993; Hornstein et al. 2000). In the retina of the male blowfly the
photoreceptors at the front of the eye have the fastest response and this is
associated with tracking (Burton et al. 2000). These variations suggest that, to
181
previously observed (Autrum 1958), it is the slower-flying insects that have
slower responses.
Fast responses are metabolically expensive because they require a membrane
with a short time constant. The membranes of fast photoreceptors contain delayed
rectifier potassium conductances that adapt the membrane for a fast response by
lowering the membrane resistance, and hence time constant. This low resistance
draws large currents. The membranes of slow photoreceptors are specialized to
reduce current (Weckstrom andLaughlin 1995). Unlike the delayed rectifiers of
fast cells, the slow cell potassium conductance responds transiently because it
inactivates. Inactivation reduces current flow and, by increasing resistance,
increases the membrane time constant. The longer time constant smooths out rapid
fluctuations in membrane voltage, but unlike fast cells, where this smoothing
would destroy fast signals, in slow cells this smoothing is advantageous (Laughlin
1996). In an insect that moves slowly and views the world through poor optics, a
rapid change in receptor response is almost certainly noise.
Fast and slow photoreceptors exemplify visual ecology in the time domain. The
dynamics of vision are matched to the dynamics of natural signals, as dictated by
life style and habitat, to strike appropriate balances between costs and benefits.
Outside of insects, comparative data is conspicuously absent, but the matching of
dynamics to life style might be widespread. Birds have higher flicker fusion
frequencies than other vertebrates (pigeon 140 Hz; chicken I 00 Hz - cited in
Laughlin and Weckstrom 1993) and there are suggestive differences among fish
(Lythgoe 1979). Matching occurs at higher levels of visual processing. The
motion sensitive neurons of hovering insects (e.g. hawkmoths and hoverflies),
respond better at lower velocities than those of insects whose flight is less well
stabilised (e.g. butterflies, blowflies and bees). Sensitivity to lower velocities is
achieved with longer time delays in motion detectors (O'Carroll et al. 1997).
Warming the retina could match response dynamics to visual ecology (Block
1986). Fast moving fish (swordfish, tuna) heat their retinas and fast moving
insects (dragonflies, honeybees) heat their heads (Heinrich 1993). Heating
improves the temporal resolving power ofphotoreceptors (Tatler et al. 2000).
The significance of economizing on photoreceptor energy usage is emphasized
by the degree to which photoreceptor response dynamics are fme-tuned.
Adaptations of response dynamics occur among photoreceptors of the same
spectral and morphological class, within one species. There are examples of a
sexual dimorphism of photoreceptor voltage response. In bibionids and in the
housefly Musca, the male has an eye region that is enlarged to detect, follow,
intercept and hopefully mate with females (Land 1997). The photoreceptors in this
male region have faster responses which, when combined with their better optics,
improves the resolution of small and rapidly moving targets (Laughlin and
Weckstrom 1993; Hornstein et al. 2000). In the retina of the male blowfly the
photoreceptors at the front of the eye have the fastest response and this is
associated with tracking (Burton et al. 2000). These variations suggest that, to