John D. Pettigrew MD
Professor of Physiology and Director of the Vision
Touch and Hearing Research Centre
Vision Touch and Hearing Research Centre
University of Queensland
Queensland 4072
Australia
+617 3365 3842 office
+617 3365 4522 fax
j.pettigrew@vthrc.uq.edu.au
I gave this wide-ranging talk as a Special Lecture to around 6000 neuroscientists at the 1997 Society for Neurocience annual meeting in New Orleans. I am gradually placing links between the different parts of the talk and adding captions to the slides, but there is a way to go.
There are 70 odd slides, so I have summarised the themes that link them
together.
Evolution has carried out many experiments on the
neural systems underlying binocular vision in vertebrates. Comparison reveals
those common aspects that may be crucial for functions like stereopsis,
as well as throwing light on the evolutionary process. Subjects include
owls, nightjars, flying foxes, reef fish and platypus.
4 MAJOR THEMES:
1.
Binocular Vision in the Owl:
Owls have evolved a mechanism for binocular vision
that is competely different from mammals. The optic nerves are totally
crossed (leading earlier authorities to pronounce that binocular vision
is impossible in owls). But there is second cross-over that brings inputs
from both eyes together in the visual Wulst, an analogue of striate cortex.
A major output of the visual Wulst is to the tectum.
Corticotectal
neurons have a very complicated pattern of projection to the midbrain tectum....in
part because a hemifield map (Wulst) has to be integrated with a full retinal
map (Tectum). One consequence of this integration is that both Wulsts project
to the same part of tectum, where the axons from both hemispheres are segregated
like ocular dominance columns...except that in this case the segregation
is based upon hemisphere of origin rather than eye of origin.
2.
Evolution of Avian Stereopsis:
Julesz conjectured that the extraordinary ability
of stereopsis to 'break' camouflage may have explained its evolution, rather
than depth judgements per se, which can be made using many other
cues. I have obtained some support for Julesz' idea by looking at stereopsis
in a range of night-jar-like
birds (based on my own chauvinistic neuroethological criteria). When
I looked at 9 different families of Caprimulgiformes (or sub-families...depending
on the taxonomist) and owls, most lacked any evidence of stereopsis in
the forebrain. Those few families with an elaborate binocular hemifield
map,. like owls, were perch-pounce strategists who took prey from the substrate.....in
contrast to all the remainder that were aerial feeeders. No other features
explained the difference between the perch-pounce substrate feeders with
stereopsis and their cortically steroblind relatives
3.
Flying Primates:
The complexites of corticotectal wiring arrangements
in the owl emphasise the dificulties of operating two systems that have
different maps of the visual world.....the whole field map of the midbrain
system and the hemifield map of the Wulst (geniculostriate) system, I used
the enormously complicated wiring diagram of the owl's corticotectal pathway
as a contrast with the sole group of vertebrates (Archontans) to wire up
the midbrain in the same hemi-decussated arrangement as the striate cortex
pathway. By bringing both the cortical and the midbrain hemifield maps
into register, Archontans
(primates and close relatives) are unique amongst mammals, since none of
the other ~20 mammalian orders have achieved this. No other vertebrate
comes close to this achievement either, not even the owls, despite the
fact that they have achieved very sophisticated hemifield maps in register
for each eyes in cortex, nor the Plethodontid salamanders who have superimposed
binocular maps in tectum.
The 'flying primate' controversy concerns my
discovery that flying
foxes (also called megachiropterans, megabats, Old World Fruit Bats)
are regular card-carrying Archontans in this respect, unlike their supposed
relatives, the microbats
(microchiropterans, fledermaus).
A heated dispute has arisen, that shows no
real sign of dying down, concerning the best explanation for this odd distribution
of characters.
Did the flying foxes evolve wings independently of
the microbats? ....In which case the Archontan hallmarks can be taken as
a true indication of their primate ancestry and we can conclude that very
early primates evolved flight in addition to all the other adaptations
for which they are famous.
Or did the flying fox and microbat really share
a common flying ancestor? ...In which case one must seek other explanations
for the large number of derived characters that are shared by flying foxes
and primates, but not by microbats.
This controversy was supposedly settled by early molecular data, but more recent and more extensive data show that the early conclusions of the molecular phylogeneticists may have been premature. (summary of molecular data on flying primates)
4. Ocular Dominance in the Platypus:
At the beginning of the talk I threw out a creative
challenge to the audience who might wonder how I could rope into a binocular
vision talk, my work on the bill sense organ of the platypus. 'What
does a marginally-sighted creature like a platypus have to do with binocular
vision?'
Even though our work on platypus electroreception
could stand on its own, there was a valid connection from platypus to binocular
visual systems. Platpus have an elaborate cortical structure that looks
rather like the ocular dominance columns of a monkey when stained for cytochrome
oxidase....except that this system of half millimetre-wide stripes is in
the somatosensory
cortex. The similarity runs deep, because the stripes
in platypus S1 allow the interdigitation of two different sensory sheets,
electrosensory and mechanosensory respectively, from the bill. Just
as the arrays for each eye may enable the measurement of very small differences
between the eyes in the interest of depth judgements, so the stripe-like
arrays in platypus S1 enable the measurement of small differences between
the time of arrival of the early electrical signal and the later mechanical
signal emanating from the tail-flick of an escaping shrimp. This
'Lightning and Thunder' arrangement enables a direct readout of the
prey's distance.
Support
National Health and Medical research Council of Australia
Australian Research Council
National Institute of Mental Health (USPHS)