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II. Retinal motion and motion perception
There are four different reasons why the image of an external object
might move on an animal's retina.
1. The object has moved
2. The animal has moved its location
3. The animal has moved its head relative to other parts of its body
4. The animal has moved its eyes relative to its head
Obviously, two or more of these could happen at the same time; and by
coincidence or by design, they might even cancel each other's effects out
so that no retinal movement results. Equally obviously, the ecological
implications of the four different types of movement are very different.
All too often, we just discuss movement perception as though all we had
to consider was the perception of a moving object by a static subject.
That is almost never the only thing that is happening, and in the case
of birds (probably the fastest moving class of vertebrates, on average)
it is certainly not the only important case. Therefore, in this chapter
we give the discussion of motion detection and recognition in pigeons a
broader perspective, but first discussing studies on the relationship of
the birds' own movements to the changing or moving image on the birds'
retina (retinal motion). The processing of retinal motion information may
be quite different depending on whether, and how, the bird itself is moving,
and it is the job for the behavioral scientist to separate these different
aspects of motion processing.
Visual stability while moving
Animals are always moving around, and most retinal image motion is
caused at least in part by movement of the animal itself. There are, of
course, compensatory eye movements that can reduce the effects of retinal
movement but they can never remove it completely. For example, during pecking
movements, when the head moves downwards, it seems that pigeons are able
to make convergent eye movements to keep the view of seeds in focus (e.g.
Martinoya, Le Hourezec & Bloch, 1984). Therefore, pigeons must be able
to distinguish between self- and externally-generated retinal motion if
they are to perceive and use visual motion information appropriately. A
moving pigeon seems to have three sources of information available about
self motion: a) visual consequences, b) motor commands, and c) proprioceptive
feedback. The task for the behaviorist and the physiologist is to find
out which information is actually used under which circumstances. For example,
the retinal motion information might be supplemented by proprioceptive
information about the position of the head with respect to the surrounding
space, of the head with respect to the body, of the body with
the surrounding space, of the eyes with respect to the world, and the eyes
with respect to the surrounding space. In order to make distinctions between
self- and externally generated retinal motion possible, it has been assumed
that an animal's movement produces information that is made available as
feedback into the visual system. Such 'reafferent'
processes were postulated and discussed by Erich von Holst and Horst
Mittelstaedt who published an extremely influential paper in 1950 under
the title "The reafference principle: Interaction between the central nervous
system and the periphery" (translated from the German).
One assumption of the reafference principle is that if the animal moves
its eyes or head, the stimulation generated by the change of the retinal
image constitutes a reafference. The stimulation is called reafference
because this information is the product of its own movement. It is distinguished
from a motion stimulation as a consequence of an object moving. Therefore,
in some way the animal distinguishes between movement of objects relative
to its eyes, when this is a consequence of its own movement, from the relative
movement as a result of objects moving externally. It is hypothesized
that self-initiated movement is triggered by a command (="move" or movement)
from a higher center which sets up an 'efference copy' or 'corollary discharge'
in a lower center. This may then send motor impulses or 'efference' to
the muscles. As a result of the movement a 'reafference' stimulation, e.g.
actual retinal motion, is compared with the efference copy in the
lower center, e.g. anticipated retinal motion. Visual stability, for example,
is achieved if the two signals compensate each other. Otherwise, orientational
movements to compensate for the discrepancy between actual and anticipated
retinal motion would follow. Independent of v.Holst and Mittelstaedt's
(1950) report that the fly Eristalis turned indefinitely when its
head was turned by 180 degrees, Sperry (1950) reported similar observations
in frogs and fishes. In these experiments the orientational coordinates
of the visual system were manipulated and as a consequence the actual visual
input and the anticipated visual input seemed always incompatible, leading
to some form of compensatory movements indeed, e.g. circling.
Although the reafference principle has been more generally applied to
kinesthetic stimulation and animal's movement in space (see v.Holst 1954)
- including our own movements, its relationship to a more complete conception
of the visual organization of the surrounding space and its cognitive implications
have yet to be fully explored. Furthermore, it can be assumed that the
different visual systems of pigeons, such as frontal visual system and
lateral visual system, might play a very different role in processing retinal
motion and that feedback about the magnetic orientation as well as the polarization
of the light rays might also be processed in this respect.
This long list of potential sources of information reminds us that the
problem of allocating retinal motion to self motion or object motion is
an extremely important one, ecologically speaking. The fact that so many
systems contribute to the solution of this problem is evidence of both
importance and its complexity. Here, the view is forwarded that visual
stability during movement is a result of the multiple interactions of visual,
efference copy and proprioceptive as well as cognitive information (see
Mergner & Rosemeier, 1998). As important as the notion of 'efference
copy' appears to be, this principle on its own does not seem to provide
a sufficient explanation of visual stability in all cases.
One of the open questions, of course, is the problem of the appropriate
coordinate system both for representing the space surrounding an animal,
and at the same time for guiding behavior. Such a coordinate system requires
a spatial reference point and procedures for spatial referencing, e.g.
a geometry. Possible reference frames could be the retina, the eyes, the
head, the body or some areas of extra-body space. Possible geometries include
the Euclidean system of three orthogonal axes, scaling the X, Y and Z dimension.
However, in the context of human visual perception such geometries have
been found arbitrary and biologically implausible (e.g. Koenderink, 1986,
Simpson, Leonard & Soodak, 1988), and these problems would even be
more severe in the case of a flying bird or a piscivorous bird with the
eyes above water to a submerged prey with its bill. The visual mechanisms
and spatial geometries of prey capture in water birds are further discussed
in Katzir (1993) and Lythgoe (1979).
In a biological context, the effective axes of spatial referencing seem
to be non-linear and non-orthogonal, and several different solutions might
be used, as long as spatial representations can be converted from one coordinate
system into another. For example, to convert from representing space based
on retinal coordinates into a body-referenced system requires information
about the position of the head with respect to the body. Such conversion
is not necessarily simple and may require additional information. Normally,
the motion of organisms or their parts in space can be characterized by
a combination of translation and rotation. The speed of translation refers
to the rate of change of distance (e.g. meters/second) and the speed of
rotation refers to the rate of change of angle (e.g. degrees/second). The
same characterization of motion can be used when referring to moving object
images on the retina. There is no single "correct" solution for spatial
referencing as long as conversion from one into another reference frame
is possible, for example from retinal coordinates into extra-body coordinates.
A convenient method for describing motion characteristics is called vectorial
representation and tries to avoid some shortcomings of the orthogonal or
linear reference systems. The
method of vectorial representation seems equally useful when describing
either the rotation of the head or body, or when describing its visual
consequences. In either case the result is a set of retinal flow fields
that can be described in vector terms. Martin Hoffman (Australian
National University) has compiled a neat self-motion demonstration
what this looks like:
The distinction between self motion and object motion has important
consequences for the organism. Therefore, it has to be robust: it must
work under a wide range of circumstances and at all times. The pigeon that
mistakes its own movement for a movement of the building it is flying towards
is in for a rude shock. As Walls (1942, p.343) put it: "No sense other than
vision is at all reliable for the orientation of animals with respect to
the objects in space. And the big reason why it is vital to know
where things are is that some of those things, and the animal itself, move."
More recent discoveries about, for example, echo-location might cause
us to qualify the first clause. At least two groups of birds are
now known to include some echo-locators (swiftlets, see for example
Griffin and Thompson, 1982, and oilbirds, see e.g. Suthers & Hector,
1985). But these remain exceptions, and in any case Walls's second
clause remains powerfully persuasive: position has to be constantly monitored
just because it changes.
In the case of object motion, movements of the retinal image may in
many cases provide the features necessary to determine the structure of
the surrounding space or the 3-D structure of objects. Walls argued that
one could not imagine vision without the capacity for motion processing.
Other abilities, such as high levels of spatial resolution, or color processing,
might be dispensable, and present in one species but not of another; but
a species that could not "make sense" out of retinal motion could barely
be said to see at all. In his rather old-fashioned terminology, Walls writes
of the great importance of the "awareness of motion". Interestingly, he
also pointed out that sessile organisms, plants or even relatives of eyed
animals like sealilies and barnacles, though they lack eyes altogether,
may still be able to respond to movement. The shell-closure reflex of barnacles
is a fine example: here the approach of a potential predator that casts
its shadow on the few photosensitive receptors, by measuring changes in
light intensity, highlighting the role of motion from an evolutionary viewpoint
at an early stage. A related point is that neurons sensitive to directional
motion are surprisingly common in the retina and optic tectum of lower
vertebrates, especially amphibians and fish (e.g. Ewert, 1982; O'Benar,
1976), compared with the situation in cats and monkeys. It seems that the
most basic (and therefore evolutionarily most essential) kinds of visual
processing involve mechanisms of motion detection.
Several studies of the optic tectum in birds, mainly of the pigeon,
show that a large proportion of the neurons are motion-sensitive with a
center-surround organization and therefore selective for relative motion
(e.g. Jassik-Gerschenfeld & Guichard, 1972; Frost & DiFranco, 1976).
However, to construct the structure of the surrounding space and objects
from a moving retinal image, the organism seems to need some knowledge
about the 3-D structure of the world including objects. It is at this end
of the process where the study of animal cognition from an evolutionary-ecological
viewpoint might be able to make a contribution, in revealing the properties
of the pigeon's knowledge about the world, and gaining an understanding
of the contribution to it of the perception of moving objects.
The role of head movements: The
"visual input enhancing" hypothesis
For example, it seems reasonable to assume that there would be a strong
relationship between a bird's typical head movements and its visual processing.
A common form of head movements in pigeons can be called head bobbing and
has been described as a thrust-hold cycle (e.g. Friedman, 1975; Frost,
1978). During the thrust phase the head is rapidly thrust forward, whereas
during the hold phase it seems as it remains virtually motionless with
respect to forward or backward movement (our clear visual impression that
pigeons retract the head at some point during the movement is an illusion).
Head bobbing movements are widespread among bird species, being found at
least in 8 out of the 27 families of birds one can find representatives
of head bobbing (Frost 1978); Dagg (1977) lists 28 species that demonstrate
head bobbing during locomotion. There are at least three ways in which
head bobbing might be related to visual processing and, surely, the different
hypotheses proposed should not be seen as exclusive:
1. The head movements may allow the birds to process some kind of visual
input which otherwise the birds would either not be able to sense or process.
In this case, head movements would generate some kind of relative motion
which is necessary if the birds is to detect or recognize objects or their
characteristics. We argue that in this case head movements do not lead
to the interruption of visual processing in some way but, on the
contrary, such head movements seem to be necessary to guarantee appropriate
visual processing. Therefore, we hypothesize that head bobbing movements
can provide opportunities for enhanced visual processing. We can call this
the "visual input enhancing" hypothesis of head bobbing.
2. Even if head bobbing has developed independently of any immediate
role in the visual processing of object information, the relative motion
images generated on the retina would still result in specific processing
requirements for the visual system - not least because the birds have to
distinguish between self-generated relative motion on the retina and externally-generated
flow patterns on the retina. We can call this the "gaze stabilizing" hypothesis
of head bobbing, as the bird has to compensate for the retinal flow in
order to maintain visual stability. Recently, it has been shown by using
videography that during the hold phase the head of pigeons is really held
stable in space (Troje & Frost, 2000). In this study the pigeon's head-bobbing
has been interpreted as an optokinetic response to stabilize the retinal
image during the hold phase.
3. A different kind of compensation process would be involved when head
movements are not shown in form of the typical head bobbing rhythm, but
in the form of adjusting head movements or some form of eye movements (e.g.
Fox 1978, Erichsen et al. 1989, Wohlschlager, Jager & Delius, 1993)
that actually serve to maintain a more constant retinal image. We can call
this the "visual compensation" hypothesis. One way of compensating for
retinal flow would be to suppress the processing of visual input during
head or eye movement altogether. In humans, this is known as 'saccadic
suppression' and a similar mechanism has been postulated in pigeons. Pratt
(1982) found that saccades were made during 80% of the thrusts of head
bobbing, and not made in the hold phase. This result leads to the assumption
that during thrusts with saccades there is probably no visual input because
retinal motion information is suppressed.
The 'gaze stabilizing' and the 'visual compensation' hypotheses both
seem to strongly imply a need to integrate signals from the vestibular
system, indicating head/body movements, with signals from the visual system,
indicating optical flow signals on the retina. Such an integration of the
two signals might result in a body velocity signal that reliably indicated
the spatial relationship of the bird to its environment. Precise information
about the bird's own spatial position in relation to its surrounding is
crucial for any visual processing of motion information. A nice example
for the relationship of head movements, locomotion and visual perception
of space can be found when chickens have to jump over gaps of different
depths and widths, walking on different surfaces and facing a visual cliff
(e.g. Green 1998a, Green 1998b). Head orientation was defined by the angle
between the horizontal and the line linking center of the eye and the tip
of the beak. The orientation was measured at the point where a jump began
based on video recordings. It was found that up to one-week old chicks
showed a consistent upward rotation of the head if the gap became wider
or if the far side was raised. According to Green head orientation seemed
independent of the fixation of the far edge at a particular elevation in
the visual field, that means any hypotheses based on specialized retinal
areas or visual field structure (e.g. myopia) might well be inappropriate.
Instead, there was a consistent relationship between head orientation and
the initial trajectory of the jump movements; each 1 degree change in trajectory
change for a potential jump was accompanied by an approximately 1 degree
change in head orientation. In such situations as jumping or landing the
relationship of head/eye movements and visual information appears crucial
for birds in controlling such parameters as body speed and direction, foot
extension during jumping and landing. But also during walking, as Green
found, head orientation seems closely correlated with the slope of
the surface, downward slope leads to an increase in head angle and vice
versa. Interestingly, the same effect was found when the animals walked
on a level transparent surface above a slope, ruling out a merely
simple kinaesthetic or motor interpretation. Therefore, here it is suggested
that head movements play a crucial role not only in gaze stabilization but often more unexpectedly in enhancing visual input.
Studying the role of head and eye movements in pigeons Wohlschlager
et al (1993) simultaneously recorded head and eye movements during locomotory
and pecking behavior. The pigeons were trained to traverse a conditioning
chamber, with a pecking key and a food dispenser at each end. Each trial
involved key pecking, walking, and feeding. Head movements were registered
with a skull-mounted miniature accelerometer, and eye movements were recorded
with implanted electrooculogram (EOG) electrodes. They found an almost
perfect temporal coordination between head and eye movements during both
walking and feeding bouts. The findings have been interpreted that during
walking, head movements primarily provide retinal image stability, and
eye movements support visual scanning. Then, during feeding, head movements
mainly subserve the grasping of food items, and eye movements maintain
visual fixation on them. These findings illustrate the 'visual compensation'
hypothesis of eye or head movements.
Of course, birds' movement perception has been studied in relation to
visual flow fields. But it seems that, in the past, birds' performance
has not been systematically linked to their own movements during perception.
In other words, the perceptual and cognitive consequences of the birds'
own movements when being tested have not sufficiently been taken into account
when discussing motion perception. In this context, it is interesting that
Frost & Nakayama (1983) have described neurons of the pigeon optic
tectum which are inhibited by in-phase motion of a small object against
a background but facilitated by anti-phase motion. The inhibitory surround
seems very large and responses seem only broadly tuned to motion direction.
These are the characteristics we would expect if these neurons are involved
in detecting relative motion of objects triggered by the bird's own motion.
But it would be a poor motion detection system that could only tell
self-motion from object-motion by the proportion of the visual field that
moved. Obviously a much better job can be done if objects in the world
can be identified, and classified as likely or unlikely to be in motion.
Conversely, the characteristic modes of motion of an object must have an
important role to play in the identification of that. Thus the remainder
of this chapter concentrates on the interaction between movement perception
in birds (mainly pigeons) and the concepts through which they categorize
the objects in their visual world. A highly interactive process seems to
be required if an organism is to simultaneously interpret self motion information
including retinal motion, on the one hand, and categorize objects, on the
other. But in the case of humans' sophisticated ability to perceive the
movements of others it has been argued that it is exactly this interactive
nature of the processing mechanisms which contribute to many of the astonishing
results in motion perception, outlined in Dittrich's (1999) 'interactive
encoding model' of movement perception. Following this line of argument,
we suggest replacing the idea of 'motion detectors' with the broader notion
of 'motion integrators' to capture the cooperative, flexible and adaptive
nature of such motion processing mechanisms, particularly in vertebrates
(for a discussion see Dittrich 1999). On this view, it is an important
task both for the behaviorist and physiologist to determine the working
principles of the motion integration centers responsible for the interactive
processing of various sources of motion information. The following sections
of the chapter give an overview of the contribution to this task from current
work on avian cognition and behavior.
Next section: Motion