The Design of Compound Eyes and the Illumination of Natural Habitats
199
be matched by an increase in Llrj>. This indeed seems to be the case in the apposition
eyes of many flying animals (Land 1999), including the hoverfly Volucella (Fig. 3):
Llrj> increases progressively from front to back.
Of course, flow-field information continues to be processed in the brain. In the
humble blowfly this occurs, in my opinion, with one of the most remarkable matched
filters of all. For more than two decades, the lobula plate of the blowfly has been
known to contain cells, known as horizontal (H) and vertical (V) cells, which respond
to wide field motion. Some cells apparently prefer upward or downward motion,
others leftward or rightward. Recently, Krapp and Hengstenberg (1996) examined
very small regions of the visual fields of these cells, and discovered that the local
direction preference was usually very different to the global preference. In fact they
found that the local preferred direction changed in a predictable manner from one
region to the next, building up an orderly map of directions across the entire visual
field of the cell (Fig. SB). The most remarkable feature of these maps is that they are
astonishingly good matches to the maps of motion vectors that describe flow fields
(Fig. SA). Cell VS6 (Fig. SB) has a map of preferred motion directions that is
extremely similar to the map of motion vectors describing roll, the field of rotating
features that results from a turn around the body axis (rotation: Fig. SA). This means
that if a fly makes a roll turn, VS6 will be maximally stimulated. Signals from these
cells can then be used to activate compensatory flight manoeuvres that correct the
fly's course. Similar matching can be found in other cells, including VSI which
matches pitch, the field of upwardly moving features resulting from a nose dive. The
cell VS8 matches a field consisting of both pitch and roll. In other words, taken as a
group, these cells respond vigorously whenever the fly experiences optic flow, an
impressive matched filter for the motion of the world.
3.2 Superposition Eyes
Finally, a discussion of eye designs in bright habitats would be incomplete without
mentioning the odd case of diurnal superposition eyes. The superposition design, the
favourite of dim habitats, is surprisingly common in diurnal insects, especially among
butterflies, moths and beetles. These superposition eyes generally have reduced
apertures (see below) but if designed properly, the extra light afforded by this design
can actually improve vision even in bright light. The aerobatic hummingbird
hawkmoth has such an eye. The eye even has local acute zones in the retina, and a
superposition aperture that is largest fronto-ventrally, in a region of the eye used for
fixating flowers during feeding (Warrant et al. 1999). Such features were previously
thought impossible for superposition eyes. Its acute zones- a horizontal visual streak
for horizon detection and a highly acute frontal zone for flower fixation - are achieved
by packing more rhabdoms into the retina than there are facets in the overlying
cornea, with up to four rhabdoms for every facet (Fig. 6). This results in a remarkable
superposition eye specialized for fixating flowers during feeding in bright light: the
brightest and sharpest image of the flower is formed on the most acute part of the
retina. Meanwhile, the visual streak aligns with the horizon to ensure stable hovering.
199
be matched by an increase in Llrj>. This indeed seems to be the case in the apposition
eyes of many flying animals (Land 1999), including the hoverfly Volucella (Fig. 3):
Llrj> increases progressively from front to back.
Of course, flow-field information continues to be processed in the brain. In the
humble blowfly this occurs, in my opinion, with one of the most remarkable matched
filters of all. For more than two decades, the lobula plate of the blowfly has been
known to contain cells, known as horizontal (H) and vertical (V) cells, which respond
to wide field motion. Some cells apparently prefer upward or downward motion,
others leftward or rightward. Recently, Krapp and Hengstenberg (1996) examined
very small regions of the visual fields of these cells, and discovered that the local
direction preference was usually very different to the global preference. In fact they
found that the local preferred direction changed in a predictable manner from one
region to the next, building up an orderly map of directions across the entire visual
field of the cell (Fig. SB). The most remarkable feature of these maps is that they are
astonishingly good matches to the maps of motion vectors that describe flow fields
(Fig. SA). Cell VS6 (Fig. SB) has a map of preferred motion directions that is
extremely similar to the map of motion vectors describing roll, the field of rotating
features that results from a turn around the body axis (rotation: Fig. SA). This means
that if a fly makes a roll turn, VS6 will be maximally stimulated. Signals from these
cells can then be used to activate compensatory flight manoeuvres that correct the
fly's course. Similar matching can be found in other cells, including VSI which
matches pitch, the field of upwardly moving features resulting from a nose dive. The
cell VS8 matches a field consisting of both pitch and roll. In other words, taken as a
group, these cells respond vigorously whenever the fly experiences optic flow, an
impressive matched filter for the motion of the world.
3.2 Superposition Eyes
Finally, a discussion of eye designs in bright habitats would be incomplete without
mentioning the odd case of diurnal superposition eyes. The superposition design, the
favourite of dim habitats, is surprisingly common in diurnal insects, especially among
butterflies, moths and beetles. These superposition eyes generally have reduced
apertures (see below) but if designed properly, the extra light afforded by this design
can actually improve vision even in bright light. The aerobatic hummingbird
hawkmoth has such an eye. The eye even has local acute zones in the retina, and a
superposition aperture that is largest fronto-ventrally, in a region of the eye used for
fixating flowers during feeding (Warrant et al. 1999). Such features were previously
thought impossible for superposition eyes. Its acute zones- a horizontal visual streak
for horizon detection and a highly acute frontal zone for flower fixation - are achieved
by packing more rhabdoms into the retina than there are facets in the overlying
cornea, with up to four rhabdoms for every facet (Fig. 6). This results in a remarkable
superposition eye specialized for fixating flowers during feeding in bright light: the
brightest and sharpest image of the flower is formed on the most acute part of the
retina. Meanwhile, the visual streak aligns with the horizon to ensure stable hovering.