H. B. Barlow

Single Units and Sensation: A Neuron Doctrine for Perceptual Psychology?

The problem discussed is the relationship between the firing of single neurons in sensory pathways and subjectively experienced sensations. The conclusions are formulated as the following five dogmas: To understand nervous function one needs to look at interactions at a cellular level, rather than either a more macroscopic or microscopic level, because behaviour depends upon the organized pattern of these intercellular interactions. The sensory system is organized to achieve as complete a representation of the sensory stimulus as possible with the minimum number of active neurons. Trigger features of sensory neurons are matched to redundant patterns of stimulation by experience as well as by developmental processes. Perception corresponds to the activity of a small selection from the very numerous high-level neurons, each of which corresponds to a pattern of external events of the order of complexity of the events symbolized by a word. High impulse frequency in such neurons corresponds to high certainty that the trigger feature is present. The development of the concepts leading up to these speculative dogmas, their experimental basis, and some of their limitations are discussed.

The neural mechanism of binocular depth discrimination

1. Binocularly driven units were investigated in the cats primary visual cortex.

Temporal and spatial summation in human vision at different background intensities

The present experiments were undertaken as part of an investigation of the suggestion made by Rose (1942, 1948) and de Vries (1943) that human visual performance is limited by the inevitable fluctuations in the numbers of quanta absorbed in the retina. In a previous paper (Barlow, 1957) it was shown that this idea (modified by assuming that there is also a weak intrinsic source of noise) leads to theoretical curves which fit experimental determinations of increment threshold made with a short duration small area test stimulus superimposed upon a large uniform adapting field. It was also shown that big changes in the amount of temporal and spatial summation occur when the background intensity is changed, with the result that when thresholds are determined with a long duration large area test stimulus the experimental points deviate from the appropriate theoretical curve and tend to obey the Weber law instead. In following up this finding there were two objectives. The quantum fluctuation hypothesis predicts that the increment threshold intensity should be inversely proportional to the square root ofthe area and duration ofthe stimulus, and the first object was to find whether the occurrence of these laws fitted in with the hypothesis: the results show that the predicted laws of summation do hold over certain ranges, but when they hold the actual values of the thresholds are higher than the theory predicts. The second objective was to determine the parameters oc and r which were introduced in the previous paper; these are the area and time over which quanta absorbed from the background light are liable to be confused with those absorbed from a short duration small area stimulus light, and here the results obtained are disappointing, for one can only derive lower limits to these quantities. On the other hand, the results do show up the complicated interrelations between temporal and spatial summation and background intensity; tentative explanations of these effects, and of the failure to perform up to the quantal fluctuation limit, are put forward. 22 PHYSIO. CXLI

Redundancy reduction revisited

Soon after Shannon defined the concept of redundancy it was suggested that it gave insight into mechanisms of sensory processing, perception, intelligence and inference. Can we now judge whether there is anything in this idea, and can we see where it should direct our thinking? This paper argues that the original hypothesis was wrong in over-emphasizing the role of compressive coding and economy in neuron numbers, but right in drawing attention to the importance of redundancy. Furthermore there is a clear direction in which it now points, namely to the overwhelming importance of probabilities and statistics in neuroscience. The brain has to decide upon actions in a competitive, chance-driven world, and to do this well it must know about and exploit the non-random probabilities and interdependences of objects and events signalled by sensory messages. These are particularly relevant for Bayesian calculations of the optimum course of action. Instead of thinking of neural representations as transformations of stimulus energies, we should regard them as approximate estimates of the probable truths of hypotheses about the current environment, for these are the quantities required by a probabilistic brain working on Bayesian principles.

Retinal Noise and Absolute Threshold

It is shown that the absorption of one quantum can excite a rod in the human retina, but that at least two, and probably many more, excited rods are needed to give a sensation of light. It is suggested that noise in the optic pathway limits its sensitivity, and this idea is subjected to an experimental test. The hypothesis is then formulated quantitatively, and shown to be able to account for the above experiment, and also the disagreement in the literature between those who believe that the absorption of two quanta can cause a sensation, and those who believe that 5 or more are required. The formulation of the hypothesis is used to calculate the maximum allowable noise (expressed as a number x of random, independent events confusable with the absorption of a quantum of light) in the optic pathway for the absorption of various fractions of the total number of quanta incident at the cornea.

Selective Sensitivity to Direction of Movement in Ganglion Cells of the Rabbit Retina

Among the ganglion cells in the rabbits retina there is a class that responds to movement of a stimulus in one direction, and does not respond to movement in the opposite direction. The same directional selectivity holds over the whole receptive field of one such cell, but the selected direction differs in different cells. The discharge is almost uninfluenced by the intensity of the stimulus spot, and the response occurs for the same direction of movement when a black spot is substituted for a light spot.

The Ferrier Lecture, 1980: Critical Limiting Factors in the Design of the Eye and Visual Cortex

The main factors limiting the performance of the peripheral parts of the visual system can be specified, and doing this clarifies the nature of the interpretive tasks that must be performed by the central parts of the system. It is argued that the critical factor that hinders development of better resolving power is the difficulty of confining light within the waveguide-like outer segment, and that for sensitivity this critical factor is the thermal decomposition of photosensitive pigments. Knowledge of these limits makes many surprising details of the eye intelligible. Understanding the difficulties posed by the narrow dynamic range of nerve fibres may give similar insight into the coding of the retinal image for transmission to the brain. Our level of understanding changes when we come to the visual cortex, for although we do not lack good anatomical and neurophysiological data, these do not make the principles of operation self-evident in the way that the structure of the eye immediately suggests that it is an image-forming device. The cortex converts the representation of the visual field that it receives into reliable knowledge of the world around us, and the trouble may be that we lack good models of how this can be done. A system that can respond to single quanta and resolve almost to the diffraction limit is unlikely to employ grossly inefficient methods for those higher functions upon which its whole utility depends, and so it is worth seeking out the limiting factors. The quality of human performance at certain higher perceptual tasks is high compared with the limit of reliable statistical inference; hence much of the sample of information available in a visual image must be effectively utilized. But there are strong limitations on the connectivity in the cortex, so that one is forced to consider how the relevant information can be collected together. Three stages of dealing with the visual image are proposed: the improvement of the cortical map in primary visual cortex by processes analogous to spatial and temporal interpolation ; the detection of linking features in this map; and the concentration of this information by non-topographical mapping in adjacent visual areas.

Changes in the maintained discharge with adaptation level in the cat retina

1. The mean rate, impulse interval distribution, and pulse number distribution of the maintained discharge of ganglion cells in the retina of the cat have been studied after prolonged adaptation at different luminance levels.

Responses to single quanta of light in retinal ganglion cells of the cat.

Abstract Under the best conditions, single ganglion cells of the cats retina give one extra impulse (average) for less than 3 quanta (average) at the cornea. A stimulus containing about 15.50 quanta at the cornea is required to reliably modulate the maintained discharge. Calculations suggest that when a single quantum is absorbed in the retina several extra impulses must be initiated. This is confirmed by the statistics of the response. For quanta absorbed in receptors in the periphery of the receptive field fewer impulses result, and this is confirmed by reduced variability of response.

What causes trichromacy? A theoretical analysis using comb-filtered spectra

For colour vision, the task of the eye is to discriminate different distributions of energy over the spectrum. This is usually treated as a problem in the wavelength domain, analogous to treating spatial resolution in terms of spatial positions in the image. What is attempted here is a treatment of colour vision in terms of the systems responses to spectral energy distributions that are sinusoidal functions of wavelength. These are called comb-filtered spectra, and the treatment is analogous to that of spatial vision in terms of spatial sinusoids. This gives some insight into the reasons for trichromacy, the advantages of oil droplets, and the narrow separation of the red and green mechanisms. It is also shown that the absorption spectra of photosensitive pigments are superimposable if plotted as a function of the fourth root of wavelength.