Haldan Keffer Hartline
(1903–1983) might always have been destined for a life in
biological research [1]. His parents
were highly educated teachers at the Bloomsburg State Normal School in
Pennsylvania; his father was a field naturalist with a Masters degree, with
experience at the Cold Spring Harbor marine biology station and who studied for
some time in Bonn and Heidelberg. His
mother, an English teacher at the school, also had a keen interest in
botany. From early on, Hartline had a
researcher’s attitude towards natural phenomena in which others might have
taken only a passing interest: after observing that bright sparks rising from a
fire left shorter trails than dim sparks, he began experiments at home to
explore persistence of vision.
As an undergraduate at
Lafayette college (ca. 1921) he began working with small land isopods (small
woodlice), quantifying their light-avoidance behaviour. This early research led to his first
published paper at the age of twenty [2].
While studying medicine at Johns Hopkins University, he was allowed
access to the Department of Physiology’s string galvanometer — an enormous
device for recording extremely small electrical currents. Hartline used the instrument to record
retinal action potentials in small vertebrates.
One day he caught a fly that was buzzing around his laboratory, and
mounted his electrodes to record from an ommatidium — Hartline quickly found
that retinal potentials from the fly were ten times larger than those in the
cat, and shifted his focus to visual responses in invertebrates.
Hartline began his work
with the horseshoe crab Limulus at the Woods Hole marine biological
station, where he continued his research on shadow reactions and dark
adaptation in small marine creatures.
Unsatisfied with the mechanically-amplified responses of the string galvanometer,
he built his own three-valve amplifier from scratch to drive a Matthews
oscillograph [3]. The increased
sensitivity allowed Hartline’s work on retinal action potentials to progress to
recordings from single fibres in the Limulus optic nerve. After quantifying the responses of single
units to spots of illumination, he noticed that ambient light in the laboratory
reduced the responses of an ommatidium and attached fibre prepared for
recording. It was a short step to show
that shading neighbouring ommatidia restored the activity of the isolated
fibre. Hartline and his lab explored the
dynamics and mechanism of this phenomena as an early description of lateral
inhibition in the retina (beaten to print by Kuffler working in the cat and Barlow
in the frog) [4, 5]. Such was their
zeal in precisely quantifying the effect of lateral interactions that they
produced a set of simultaneous equations that accurately describe the responses
of a set of nearby ommatidia.
Two productive decades
followed their initial observations; their work cemented the idea that the
retina does not merely transmit counts of incident photons to the brain, but
actively filters and processes incoming stimuli. The visual phenomena of Mach bands (see
figures at left) illustrate that our perception of the visual world is illusory
from the moment of sensation.
Based on the work of
Hartline and others in the retina, the concept of lateral inhibition has been
extraordinarily pervasive in neuroscience.
Models describing not only visual processing [8], but also development
of cortical maps [9] and dynamic activity in cortex [10] all stem from
Hartline’s observations. In the retina,
lateral inhibition underlies spatial and temporal contrast enhancement, as
described in detail by Hartline and his colleagues. In networks of neurons, lateral inhibition
can perform sharpening of neural representation, decision making via
competitive mechanisms, auto-associative memory storage, noise rejection, and
so on [6]. Many abstract models of
cortex adopted widespread inhibition as an anatomical fait accompli, and
continue to do so in spite of the weight of evidence against long-range
inhibition in cortex. Aside from
consistency with existing theoretical literature, this is probably due to the
computational power conferred by lateral inhibitory interactions.
Hartline was awarded
the Nobel Prize in Physiology or Medicine in 1967, along with Ragnar Granit and
George Wald, for his “discoveries of the most fundamental principles for data
processing in neuronal networks which serve sensory functions. In the case of
vision they are vital for the understanding of the mechanisms underlying
perceptions of brightness, form and movement.” [7]
Mach Bands In the 1860s, the
Austrian physicist Ernst Mach recognised that the illumination at a point on
the retina is not perceived objectively, but only in reference to its
neighbours. The optical illusion shown
at left illustrates this phenomenon: although there is a simple linear gradient
from light to dark in the centre of the image, we perceive a brighter band at
the left edge of the gradient, and a darker band at the right edge. Physiologically this effect is due to the
changing influence of surround inhibition across the image. Mach interpreted this phenomenon quite
philosophically, claiming that our perception of the world is always relative
to other stimuli; that our impression of unchanging events is actively weakened,
with the effect of enhancing the importance of events that change temporally or
spatially.
- D.R. Muir
References and further reading
[1] R Granitt and F
Ratliff, 1985. Haldan Keffer Hartline. 22 December 1903–18 March 1983. Biographical
Memoirs of Fellows of the Royal Society 31, pp 262–292.
[2] HK Hartline, 1920. Influence of light of
very low intensity on phototropic reactions of animals, J General Physiology
6 (2), pp 137–152.
[3] HK Hartline, 1974.
Foreword. In: Studies on excitation and inhibition in the retina, Eds: F
Ratliff and HK Hartline, pp xiii–xx. Rockefeller University Press, New York.
[4] HK Hartline, 1949. Inhibition
of activity of visual receptors by illuminating nearby retinal areas in the Limulus
eye, Federation Proceedings 8 (1), p 69.
[5] HK Hartline, HG
Wagner and F Ratliff, 1956. Inhibition in the eye of Limulus, J General
Physiology 39 (5), pp 651–673.
[6] RJ Douglas and KAC
Martin, 2007. Recurrent neuronal circuits of the neocortex, Current
Biology 17 (13), pp R496–R500.
[7] CG Bernhard, 1968.
In: Les Prix Nobel en 1967, Ed: R Granit. Nobel Foundation, Stockholm.
[8] G Sperling, 1970. Model
of visual adaptation and contrast detection, Perception and Psychophysics 8
(3), pp 143–157.
[9] C von der Malsburg,
1930. Self-organization of orientation sensitive cells in the striate cortex,
Kybernetic 14, pp 85–100.
[10] HR Wilson and JD
Cowan, 1973. A mathematical theory of the functional dynamics of cortical
and thalamic nervous tissue, Kybernetic 13, pp 55–80.
