Early Work on Avian Eye
Movements: My friendship and
collaboration with Josh began more than 3 decades ago. Less pecunious than I
had been in the US, I was looking for an inexpensive search coil system to
record the eye movements of exotic Australian birds. Josh had heard about this
somehow and at first suggested a DIY electronics solution. In the end, he
decided to come “down under” so that he could help me personally with its
construction. I never got around to asking him for his motivation in travelling
so far to work with a stranger, but looking back I think that the attraction
was the birds. I had just published my work on owls, so the prospect of working
on avian binocular vision may also have been a factor.
We studied many bird species, implanting a stainless steel wire under
the conjunctiva of both eyes using a modified aneurysm needle. Perhaps the most remarkable bird was the
Tawny Frogmouth, Podargus, which
adopts a camouflage posture that is so effective that one can walk within a few
feet without realising that the “broken branch” is actually this bird.
Josh and I discovered that the
camouflage posture is accompanied by a strikingly different visual mode, where
the single binocular foveas are so widely divergent that there is a blind zone
straight ahead! Aborigines took advantage of this to approach the perching bird
unseen from straight ahead,…….. only to circle around if being spied by the bird’s lateral gaze,
……..so eventually catching it by this repeated process. When a tame bird is
tempted with a food item, a different mode is adopted. Both eyes swing forward
so that both foveas now regard the morsel in front and there is significant
binocular overlap.
The brain of the frogmouth is very owl-like, with a huge visual Wulst
armed with stereo-enabling binocular neurons like the owl. This ancient
owl-frogmouth link is supported by some wide-ranging molecular studies such as
DNA-DNA hybridisation, although not by single gene phylogenies.
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Two Modes of Visual Behavior
In the Tawny Frogmouth, Podargus.
Josh’s search coil apparatus enabled the discovery of a binocular,
frontal mode (upper) that is adopted when a tame bird is not alarmed
and is
presented with food: the divergent,
defensive visual mode
(lower) is adopted along with the camouflage posture
during a threat.
In the latter posture, the divergence of the visual axes may
be so
great that there is a blind area straight ahead.
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The binocular-frontal vs. divergent-defensive modes of visual behaviour
recall the two systems conceived by Karten and Hodos from their work on avian
visual pathways. We prefer to give their “thalamofugal system” a different
name, the geniculostriate (because the tectofugal system also has a thalamic
relay and because its forebrain destination in the Wulst is an obvious analogue
of the mammalian striate cortex, even showing a “stria” in fibre stains). The
geniculostriate system is the only sensory pathway to skip over the midbrain
without a relay there, presumably because its binocular function would be
compromised if there is too much prior processing of the monocular images
before they are compared. The wiring of the tectofugal pathway (horizontal
streak of highly specialised retino-tectal ganglion cells; input largely from
the monocular fovea in those birds with two foveas; well-developed even in
those birds lacking specialisation for binocular vision) is clearly designed
for all eccentricities, not just the binocular field.
We never got around to checking the physiology to see if the tectofugal
system (or part thereof) is turned off in some sense when the frogmouth is in
binocular mode, and vice versa. It is a good bet that the geniculostriate
system is turned off when the defensive, presumably tectofugal mode, is
operative because binocular vision is an impossibility in that mode. The two
systems have a problem with registration with each other, because the
geniculostriate system has a hemifield representation compared with the whole
field representation of the tectofugal system. This must cause some kind of
clash, or rivalry, when the geniculostriate sends its massive projection back
to the tectum. A neural switch between the two systems must therefore underly
the striking switch in visual behaviour.
The frogmouth entertained Josh in the wild as well as in the lab. It
also later earned Josh a front cover article in Nature (avian saccadic oscillations, see below).
The Chilean Connection:
Josh has had 3 brilliant Chilean PhD students over the years since
1982. I played a role in this, as I was in Santiago in 1981 and steered the
first one toward Josh. He was a poet-scientist called Juan-Carlos Letelier.
Having blazed the trail from Chile to Josh’s lab in NY, Juan-Carlos was
followed by Gonzalo Marin and Ximena Rojas. They all came from a very creative
school of biological thought that had been created by Humberto Maturana at the
University of Chile. Maturana is perhaps best remembered for his co-authorship
with Jerry Lettvin and others of “What the frog’s eye tells the frog’s brain”,
but is also noted for his concept and widely translated book on “Autopoiesis”
with the late Francisco Varela. Maturana is still very active, in his 70s,
successfully treating pain in human sufferers using philosophy!
A vivid account of the way Maturana inspired students can be found at http://biologyofcognition.wordpress.com/about/
Juan-Carlos and Gonzalo, along with Jorge Mpdozis, uncovered an
extraordinary, high speed attentional system in the bird’s midbrain that is
centred on the isthmi nuclei. As often happens when a discovery is made in the
Southern Hemisphere, this finding has been taken up by some in the North
without due credit being given to the originators. Josh and I worked in
Santiago at the Maturana lab complex with the three Chileans. I think our
experiment is worth a brief description because all our data were subsequently
destroyed in a fire, along with all the other data and equipment in Maturana’s
famous laboratory.
The experiment was not
too dissimilar to receptive field plotting, except that we were using single
units to plot the path taken by an attentional spotlight, produced by the
nuclei isthmi, as it moved over the surface of the tectum. The activation
produced by the attentional spotlight has an oscillatory signature that is
unmistakeable, both to one’s eye looking at the oscilloscope, and one’s ear
listening to the speaker, when one is recording from a microelectrode. By
placing a dozen microelectrodes over the tectal surface, we could observe their
sequential activation by the “spotlight” and refer this to the equivalent
spatio-temporal pattern of the spotlight in space. We had yet to define how, or
even whether, the pattern might be affected by visual stimulation, but even
without a visual stimulus, we could observe that the spotlight tended to start
in the tectal area that corresponded to the fovea and then execute a rough
spiral to activate increasingly peripheral retinal regions. This sequential
pattern was repeated about 30 times/sec.
Another example of the
creativity of the Chileans in the environment that Josh provided in NY was
Ximena Rojas’ discovery that avian hair cells can regenerate, unlike their
mammalian counterparts. Full credit must go to Ed Rubel for pursuing this
important line of research, but I think that it is worth noting that the first
observation may have taken place under Josh’s influence.
Saccadic Oscillations:
Perhaps the most bizarre phenomenon that Josh and I worked on, along
with Chris Wildsoet, is the saccadic oscillation shown by all birds. During the
jump, or saccade, from point A to point B, the eye movement of a bird
oscillates rapidly around the rough optical axis of the eye. The frequency of
the oscillation is a function of the eye size, with the tiny eye of a zebra
finch oscillating at 60 Hz and the large eyes of nocturnal birds like owls and
stone curlews oscillating at around 10 Hz. We put this uniquely avian feature
together with another one, the avian pecten, a beautiful folded vascular
structure that projects into the eye like a keel from the region of the optic
nerve head. It is well known that the pecten provides the major nutrient supply
and waste disposal for the inner avian retina, which lacks its own blood supply
like the retinal circulation found in the more complex, thicker, mammalian
retinas. If diffusion from the pecten is the main source of nutrients and the
main exit for wastes, a significant problem would be the time taken for
diffusion. In the large eyes of nocturnal birds, unassisted diffusion from the
pecten to the edge of the retina would take many minutes. We reasoned that the
oscillating pecten would act as a stirrer, like the rotor in a washing machine,
to facilitate diffusion. The stirring would be helped by the fact that the
posterior third of the avian vitreous is liquid, unlike the gel found further
forward in birds and completely filling the vitreous of other vertebrates. The
experiment we did was simple……fluorescein angiography……and had a striking
result. Fluorescein accumulated around the base of the pecten between saccades,
but was distributed across the whole retina during the oscillations of a
saccade. The frogmouth was crucial for our success because it suppressed
saccades for long periods when it was in its defensive mode, a behaviour that
had presumably been selected to reduce the conspicuity of its large yellow
irises when under threat in the camouflage posture. In chickens we found that
the intersaccadic interval was too brief to see clearly what happens to the
fluorescein between saccades.
Hans Ussing was the living
expert in biological diffusion processes and invented the famous Ussing
chamber. When he visited and heard our story about saccadic oscillations, he
laughed in astonishment. “Only evolution can have invented such a bizarre
solution to a problem, but I believe that you are right in your
interpretation”.
Nature shared a similar
viewpoint to Ussing and published the study, along with a front cover.
Avian Model of Myopia:
If one uses as a guide the difficulty we experienced in getting
Australian grant support for working on myopia in chickens, Josh’s greatest
accomplishment must be the wide acceptance of his avian model system for
studying myopia. The rapid growth of the chick eye means that one can gather
data on the control of eye growth in weeks, as opposed to the years required to
acquire similar data in primates. The significance of the problem is brought
home by the fact that virtually every adolescent in Singapore and Hong Kong has
myopia. A fundamental understanding of this excessive eye growth phenomenon is
a key to any progress in prevention.
Josh deserves full credit for having provided the superior avian model
system that offers the best hope of providing fundamental knowledge that could
underpin a preventative strategy.
One significant
advance made by Josh in this area was the realisation that the eye itself is
capable of regulating its own growth locally, without any intervention from
outside influences, such as the brain. There was an Aussie connection here, as
Chris Wildsoet and I were interacting with Josh at the time. Teams in both
countries carried out different experiments showing that eye growth control was
local. We showed that excessive eye growth continued apace, even when the optic
nerve was sectioned. At the same time Josh and team showed that excessive
growth could be produced in a localised area of the eye if patterned vision was
prevented there……. but growth was normal in the same eye in the region with
patterned visual input. The discovery of local growth control marked a turning
point in the field, which is presently waiting for another such turning point,
one that will doubtless be delayed by Josh’s passing.
Rock Art In the Kimberley:
Bradshaw paintings are restricted to sheltered walls of Kimberley
sandstone in NW Australia and have a delicate technique that betrays a precise
observation of the natural world, as well as the ability to depict it. While on
an expedition to the Kimberley with Father Anscar MacPhee and Marilyn Nugent,
Josh and I discovered a depiction of small megabats of a species that is not
presently found in Australia. None of the 7 extant megabat species in Australia
has a white stripe on its face like those in the clear rock art depictions.
This kind of rock art is controversial because it is not clear who was
responsible, nor when, although there is little doubt that they are very old,
from the Pleistocene. I now devote myself full-time to the study of this rock
art and have had numerous fruitful conversations with Josh, whose open and
brilliant mind always helped my investigations to progress.
Josh as experimentalist in life and lab:
I have gone into a lot of detail about the experiments that I shared
with Josh because they are important parts of my memory. We both had a great
love of birds that helped to ignite our efforts in the lab, but this was a
source of joy and solace for both of us in the wild as well. We were both “slow
switchers” who sometimes suffered from the moody blues, although I was more
likely to switch the other way, toward mania. Josh had found a number of
solutions for the blues, of which “neophilia” was paramount. He would seek out
some completely new activity, challenging if possible. Travel to an exotic
location often featured. Both of us could be lifted by wild birds, so the
combination of a new avian, and a new exotic, experience was especially
therapeutic. I can remember occasions where I received from Josh an email photo
of some unusual bird he had taken in an unusual location, like the
batrachostomid frogmouth from Malaysia. This was a distant relative of the much
larger Australian frogmouth, Podargus,
that was so important for the success of our early experiments together. One
might say that our connection to birds was a spiritual one which may offset the
matter-of-fact nature of this piece.
Emeritus Professor JD Pettigrew FRS
Queensland Brain Institute
26 April 2012
Jack Pettigrew
Queensland Brain Institute
26 April 2012
